Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions.

PHYSIOLOGICAL REVIEWS Vol. 72, No. 3, July 1992 Printed in U.S.A.

Golgi Tendon Organs in Mammalian Skeletal Muscle: Functional Properties and Central Actions Li?NA

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Centre National de la Recherche ScientiJique, Unite’ de Recherche Associe’e 1448, Laboratoire de Neurophysiologie, &!16ge de France, Paris, France

I. Introduction ......................................................................................... II. Morphology .......................................................................................... A. Location .......................................................................................... B. Structure ......................................................................................... C. Trajectories of Ib fibers within the spinal cord ................................................. D. Development of tendon organs .................................................................. III. Distribution .......................................................................................... A. Numbers of tendon organs in various muscles .................................................. B. Ratios of motor units to tendon organs ......................................................... C. Ratios of tendon organs to spindles ............................................................. D. Association of tendon organs with other receptors ............................................. IV. Transduction ......................................................................................... A. Mechanical properties of tendon organs: stress and strain ..................................... B. Receptor potentials .............................................................................. C. Impulse initiation ................................................................................ V. Encoding Properties ................................................................................. A. Passive muscle stretch is not the adequate stimulus for tendon organs ....................... B. Specific stimulus: contraction of in-series muscle fibers ........................................ C. Activation of tendon organs by single motor units ............................................. D. Responses to combinations of motor units ...................................................... E. Unloading of tendon organs by contraction of in-parallel muscle fibers ....................... F. Ensemble discharges of tendon organ population from a muscle ............................... G. Nonlinearity of tendon organs: summary of causes ............................................. VI. Discharges of Tendon Organs During Natural Movements ........................................ A. Methodological problems ........................................................................ B. Records obtained in freely moving animals ..................................................... C. Human tendon organs ........................................................................... VII. Central Actions of Tendon Organs .................................................................. A. Methodological problems related to the difficulty of selectively activating Ib fibers ........... B. Spinal cord ....................................................................................... C. Cerebellum ....................................................................................... D. Cerebral cortex ................................................................................... E. Perception ........................................................................................ VIII. Conclusions ..........................................................................................

I.

INTRODUCTION

Golgi tendon organs are contraction-sensitive mechanoreceptors of mammalian skeletal muscles innervated by fast-conducting Ib afferent fibers. With this clear-cut definition, tendon organs are a challenge for functional analysis, mainly because of specific difficulties met in their study, as is spelled out in this review. In addition, the picture is blurred by lingering erroneous ideas about tendon organs. The aim of this review is therefore double: first, to expose the reasons, drawn from recent work, why old views should be abandoned; and second, to compile the data obtained by 0031-9333/92 $2.00 Copyright 0 1992 the American Physiological

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various experimental approaches that point to a possible function for these highly sensitive contraction sensors. Control of posture and movement requires permanent monitoring of muscle length and tension, which is provided in mammalian muscles by two kinds of mechanoreceptors, spindles and tendon organs, that are sensitive to changes in muscle length and tension, respectively. The term “tension” (i.e., the constrained condition resulting from the elongation of an elastic body) is used in physiological studies to designate the force that has to be opposed to a muscle to maintain it at a given 623

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length. When a noncontracting muscle is extended, it develops, by virtue of its elastic properties, a “passive tension.” By analogy, the term “active tension” is often used to designate the force developed by contraction. Both active and passive tensions are usually measured with force transducers (strain gauges) and are often expressed in “gram” units rather than Newtons, dynes, or gram-force. Given the mechanical properties of muscle tissue, length and tension are physically inseparable parameters, but while spindles monitor muscle length rather than tension (see Ref. 229), assessment of muscle tension rather than length is considered to be the task of tendon organs (occasionally termed, in early studies, musculotendinous end organ, Golgi organ, or tendon spindle). However, tendon organs are not equally sensitive to passive and active tensions. In recent years the most important advance in our knowledge of tendon organs was the demonstration that contraction is their adequate stimulus and that an individual receptor can monitor the activity of a single motor unit (156). Commonly accepted ideas that have to be revised represent the tendon organ as a stretch receptor with a high threshold and a low dynamic sensitivity. In fact, muscle stretches do not consistently or significantly activate tendon organs, whereas contraction does. Moreover, tendon organs display a very low threshold and an appreciable dynamic sensitivity when tested with their adequate stimulus: they can signal very small and rapid changes in contractile force. This is likely to have functional consequences that are not yet fully appreciated. It should also be realized that, notwithstanding their denomination, tendon organs are not located within tendons. As originally reported by Golgi (108,109), they are mostly found at points of attachment of muscle fibers to tendinous tissue, including deep intramuscular tendons or aponeuroses. This widespread distribution allows the monitoring of contractions in every portion of the muscle so that the activity of virtually every motor unit in a muscle can be signaled by at least one tendon organ. Among the specific difficulties of tendon organ studies, a first major problem is related to the fact that the contractile forces applied to individual receptors are not measurable. For this reason, it is not yet clearly understood which parameter of contraction is actually encoded by tendon organs and which information is sent to the central nervous system by Ib afferent discharges in addition to information on variations of contractile force. The second major problem met in studies of the central actions of tendon organs is the great difficulty of selectively activating Ib afferent fibers whether by electrical or by natural stimulus. Reflex effects of tendon organ afferents are therefore difficult to recognize. Early demonstrations of Ib afferent actions on motoneurons mostly rested on indirect evidence, but the main conclusions, pointing to autogenetic disynaptic inhibition of homonymous and synergic motoneurons and to excitation of antagonist motoneurons (ZOl), have been largely confirmed. Recent studies have shown that there is no “private” pathway for Ib input at the seg-

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mental level, since a variety of peripheral and central inputs converge on the interneurons mediating autogenetic inhibition (128). Information from tendon organs is coprocessed with information from other receptors and dispatched, as from a turntable, via different “alternative pathways” selected by descending motor commands (142,216). One ascending pathway, via a component of the dorsal spinocerebellar tract (DSCT), carries the information from tendon organs to the cerebellum and to the cerebral cortex (240,241,252). The fact that inputs from tendon organs reach the cerebral cortex suggests that they contribute to conscious sensations, allowing assessment of the force developed in a voluntary contraction (285). It is difficult to disentangle the relative contributions of spindles, tendon organs, and other muscle receptors, but it seems likely that all these contributions are coprocessed at the highest level, as in the spinal cord, in light of centrally generated information derived from motor command (233). This review concentrates on tendon organs of mammalian limb muscles, leaving out those of respiratory (see Ref. 76) or masticatory (see Ref. 212) muscles as well as the receptors of extraocular muscles (P. Buisseret, unpublished data). Data on the tendon organs of submammalian vertebrates can be found in the review by Proske (272). II.

MORPHOLOGY

Two main methods are employed for determining the presence and numbers of tendon organs in a muscle and for studying their structure with light microscopy. One method utilizes mechanical dissociation by teasing the surrounding muscle fibers from the receptors after impregnation with silver, gold, or osmium compounds (e.g., see Refs. 16, 73,107,306,339) or after staining for cholinesterase (313). The other method rests on systematical examination of serial cross sections of whole muscles after various preparations or after embedding in paraffin and plastic polymers (e.g., see Refs. 212, 325). Some authors have used both methods in conjunction (341). Tridimensional reconstructions were obtained from serial sections of either light (e.g., see Refs. 35,281) or electron microscopy material (248, 304, 305). Data from ultrastructural studies in rats (246, 344), mice (309), cats (304,310), and humans (248) point to common features of tendon organs among different species. A. Location

Golgi tendon organs are found in nearly all mammalian limb muscles. Very small muscles such as the tenuissimus were reported to lack tendon organs (256), but occasional instances were seen by Eldred et al. (88), and R. W. Banks found, in one muscle, two tendon organs located near the proximal origin (personal communication). Tendon organs are also present in axial mus-


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cles of the neck (279) and tail (lo?‘), as well as in masticatory (212) and respiratory muscles, including the diaphragm (68, 339; see Ref. 76). It is clear from the initial description by Golgi (108, 109) that tendon organs, which he called “musculo-tendinous end-organs,” are located exclusively at muscletendon or muscle-aponeurosis junctions and not within tendons. In the material of Pang [quoted by Barker (17)], which is the largest sample ever studied, 92.4% of 1,337 receptors from different thigh, shank, foot, and intercostal muscles of the cat were located at musculotendinous junctions versus only 7.6% within the tendon proper. The functional properties of these purely tendinous receptors are not known. Musculotendinous junctions occur not only at either end of a muscle but also on the inner side of aponeuroses and on tendons penetrating in the depth of pennate muscles. The tendons of insertion of peroneal muscles or of flexor carpi radialis, for instance, have long band-shaped intramuscular portions terminating within a few millimeters from the osseous origin of the muscle, and tendon organs are found all along these tendinous bands, mostly on their margins (281, 306). The receptors of pennate muscles are mainly concentrated close to the point of nerve entry, usually toward the proximal end of the muscle (19). In muscles with fibers slanting from an aponeurosis of origin to an aponeurosis of insertion, such as soleus, tendon organs are attached to the inward surfaces of these aponeuroses and are scattered over wide areas (313,325). Dorsal muscles of the neck, such as splenius, biventer cervicis, and complexus, are traversed by tendinous inscriptions that are not attached to bone or tendon and contain numerous tendon organs through which short muscle fibers insert into the inscriptions (279). Tendon organs, as well as spindles, were reported to occur preferentially in a central zone of the muscle termed the muscle core (212, 281, 306). In certain muscles the core contains relatively higher proportions of slow oxidative fibers than other zones in which fibers of different histochemical types intermingle homogeneously (110, 342). The vicinity of receptors and oxidative fibers might have a functional significance that is not yet ascertained (see Ref. 281). B. Structure

Tendon organs are encapsulated corpuscles innervated by large afferent fibers. Their main component is an elongated fascicle of collagen bundles attached at one end to the individual tendons of a small fascicle of muscle fibers while the other end is in continuity with the whole muscle tendon or aponeurosis (see Ref. 276). Each receptor is thus placed “in series” with a group of muscle fibers, whereas other fibers, much more numerous, coursing “in parallel” with the tendon organ body insert around its tendinous or aponeurotic end (Fig. 1). In the sample of Pang, 63% of 1,278 tendon organs had a fusiform shape; the others were bifid or trifid at one or

625

ORGANS Muscle 1’ in

parallel

”

fibers ” in

series

”

nor toll

FIG. 1. Schematic representation of tendon organ. Capsule is shown in longitudinal section. Sensory terminals are represented by knobs at end of unmyelinated branches of Ib axon. Note unequal distribution of terminals to collagen bundles within capsule. For further description see text. [Adapted from Zelena and Soukup (344).]

both ends (17). Similar figures were found for rat tendon organs of soleus and extensor digitorum longus muscles (313). The variability of sizes among tendon organs from different muscles is illustrated by the wide range of lengths (242-1,045 pm, mean 521.4 pm) and diameters (66-220 pm, mean 125.5 pm, measured at the midsection) found by Pang in 100 tendon organs. Variations in size occur also within individual muscles (306). An important parameter for the mechanical properties of tendon organs, and for the stress-strain relation (see sect. IV), is the ratio of diameter to length. This parameter has not been systematically investigated, but the available data suggest appreciable differences among individual muscles, even bearing in mind that different conditions of histological preparations may partly account for these differences. In the extensor digitorum brevis, tendon organs have an average length of 1,110 pm, and their average diameter is 56 pm (36). Similar numbers were reported for tendon organs in dorsolateral muscles of the tail, with mean lengths of 700-1,000 ,urn and mean


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diameters of 60-80 pm (107). In masticatory muscles, tendon organs are rather short (loo-310 pm in temporalis and ZOO-600 pm in masseter), but, with diameters of 30-80 pm, they are as thick as in other muscles (212). Diameters of 70-150 pm were measured at the midsection of tendon organs in flexor carpi radialis (281). Rat tendon organs have an average length of 640 pm and a diameter of 47 pm (36, 313). The corresponding dimensions are 1,600 and 122 pm, respectively, for human tendon organs (36). The body of the tendon organ is enclosed in a 3- to 12-pm thick (254) lamellar capsule that is continuous with the perineural sheath of the innervating Ib axon (296). The capsule wall, consisting of -5-20 concentric layers of cells, leaves but a narrow space around the collagen bundle and seals this space by tight collars at both ends (304). Capsular lamellae, invested by basal lamina on both sides, contain pynocytotic vesicles and show points of adherence to one another at specialized membrane zones (248). Between the layers of the capsule are collagen fibrils, microfibrils, and capillaries. The intracapsular lumen is divided into longitudinal compartments by septal lamellae derived from the innermost capsular cells. Septal processes are usually discontinuous, allowing communications between compartments. Three types of compartments can be distinguished by their content (248, 304, 344), namely, I) neural compartments usually containing the myelinated axon and axonal branches after their penetration in the lumen, Z) neurotendinous compartments containing collagen bundles and unmyelinated sensory terminals, and 3) tendinous compartments with scarce innervation or, quite frequently, without innervation at all, constituting a built-in basis for the in-parallel effects observed in tendon organ responses to certain stimuli (see sect. vE). Of 10 rat tendon organs examined by Zelena and Soukup (344), the only one that lacked a purely tendinous noninnervated compartment had a compact collagenous compartment with a single sensory terminal. At the “muscle end” of a tendon organ, the collagen bundles are connected to individual muscle fiber tendons, and at the “tendon end” they blend with the whole muscle tendon or aponeurosis (Fig. 1). In between, the fibrils from different individual tendons divide, mix, and fuse so that a compartment, whether neurotendinous or purely tendinous, may contain an assortment of fibrils connected to different muscle fibers, and the number of fibrils exiting from the capsule at the tendon end is significantly smaller than the number entering at the muscle end (304). Within the tendon organ, collagen fibrils have much smaller diameters (25-90 nm) than in tendons or aponeuroses (130-200 nm). Minimal diameters are found in purely tendinous compartments where fibrils are densely packed in bundles of regul ar shapes, circular or oval, ti ghtly pressed toge ther. In neurotendinous compartmen ts, th .icker fibrils form loosely arranged bundles of irregu lar sh apes arround the sensory terminals (344). Each tendon organ is usually innervated by a single

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fast-conducting Ib afferent fiber. Measurement of the conduction velocities of functionally identified afferent fibers is the only possible approach to an estimation of their diameters close to the spinal cord. The conduction velocities of fibers supplying tendon organs and spindle primary endings in triceps surae muscles, respectively termed Ib and Ia, were systematically measured by Hunt (163) and found to range between 60 and 110 m/s, with complete overlap of tendon organ and spindle afferent conduction velocities. However, among the fastest afferents, there are less Ib than Ia fibers. This was very clearly shown by Laporte and Bessou (200) in the nerves to posterior biceps and semitendinosus m.uscles of cats. With the use of the conventional conversion factor of Hursh (diameter in ,um X 6 = conduction velocity in m/s), the estimated range of Ib fiber diameters falls between 10 and 20 pm (163). In the vicinity of receptors, there is also an overlap between the diameters of Ia and Ib fibers (1). Close to the tendon organ, Ib fibers have diameters of 7-14 pm (Pang; earlier references quoted in Ref. 17; see also Refs. 35,341). In the sample of Pang, only 1.8% of 1,062 tendon organs were supplied by two apparently independent Ib fibers. There was a higher incidence (15%) of Ib fibers dividing to supply two or three receptors. In cat tail muscles, 4-30s (mean 16%) of tendon organs are innervated by a fiber that also innervates a second tendon organ , and less numer ‘OUS (4 % ) “aff eren t units” include three tend on organs (107). Occasional innervation of two tendon organs by a single Ib axon also occurs in peroneal muscles (306). The Ib fiber often divides in two or three myelinated branches before penetrating the capsule near the middle of its length, and the daughter branches in turn divide within the neural compartment of the capsule. Further branches eventually shed their myelin and enter the neurotendinous compartments where their terminals are interwoven among braided collagen strands (248,304). The terminals are densely packed with mitochondria and form enlargements, sending lateral projections that increase the surface of contact between neural membrane and collagen bundles (248, 304, 305, 344). As mentioned, contacts between sensory terminals and collagen bundles are not evenly distributed within the capsule: the so-called neurotendinous compartments contain many more contacts than the tendinous compartments. The functional significance of the additional innervation of tendon organs by small-diameter (2-3 pm) myelinated fibers, first reported by Ruffini (295), is not yet understood. Some of these “concomitant,” “accessory,” or “satellite” fibers (see references in Ref. 17) are clearly afferent, since they persist in deefferented and sympathectomized preparations, terminating with free endings in various locations either within or without the tendon organ capsule (316, 317). According to Barker and Saito (20), sympathetic innervation is lacking in tendon organs. The number of muscle fibers attached in series with a tendon organ varied in a range of 3-50 in the sample of


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Pang, but only 5% of 1,337 receptors had >25 fibers (17; see also Ref. 36). This has been largely confirmed by data from various cat muscles, such as extensor carpi ulnaris [22 fibers (304)], extensor digitorum brevis [lo20 fibers (35)], soleus [13-41 fibers (315)], and peroneal muscles [4-26 fibers (306)]. In tail muscles, a significant correlation was found between the number of fibers (in a range of 3-22) in series with a tendon organ and the width of the capsule (107). Rat tendon organs have 5-10 muscle fibers attached in series (36,344), and in human muscles, complements of lo-20 fibers have been reported (36). The myotendinous junctions of the in-series fibers lie at various distances from the tendon organ, with individual tendons converging toward the capsule collar where they fuse in three or more bundles in a funnellike shape (315, 344). A peculiarity of muscle fibers in series with tendon organs of long strap muscles is that they do not run the whole length of the muscle. In the cat sartorius, fascicles are ~10 cm long, but many muscle fibers have lengths of only 2-3 cm, tapering in thin ends apposed to the surface of neighboring fibers. Fibers connected to tendon organs located at myotendinous junctions can be as short as 1.4-2.4 cm and terminate intrafascicularly in the same fashion (210). In addition to the muscle fibers attached in series with the tendon organ, a large number of fibers run in parallel with the receptor, inserting around its tendinous or aponeurotic end. The functional significance of these fibers is important because, as explained in detail in section vE, their contraction tends to reduce the strain on the eollagenous bundle and on the sensory terminals, i.e., to “unload” the tendon organ. In a detailed account of the structure of tendon organs from rat shank muscles, Zelena and Soukup (344) drew attention to the fact that some muscle fibers, which are apparently in series with a receptor, must in fact exert in-parallel influences on their sensory terminals because their tendons of insertion remain, within the capsule, in purely tendinous compartments that are either poorly innervated or completely devoid of innervation. Other instances of pseudo-in-series attachment can be provided by a muscle fiber and its tendon forming a noninnervated head in a bifid tendon organ. Both heads of the tendon organ have their independent inner capsule, but they are enclosed in common outer capsular layers. The noninnervated compartment obviously constitutes a functionally in-parallel component within the tendon organ itself. It also occurs that a muscle fiber running along and just outside of the tendon organ body will insert its tendon into the capsular wall, either in the upper or in the lower half of the body length (36, 315, 344), and this attachment is likely to produce in-parallel effects when the fiber contract. The vascular supply to tendon organs is provided by branches of the blood vessels that enter the capsule together with the nerve. According to Nitatori (248), capillaries do not enter the compartment where sensory terminals contact collagen bundles, i.e., where transduction of mechanical stimulus into electrical signal takes place.

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C. Trajectories of Ib Fibers Within the Spinal Cord

After penetrating in the spinal cord, Ib afferent fibers from hindlimb muscles divide in ascending and descending branches, giving off collaterals at several segmental levels. The ascending branch travels in the ipsilateral dorsal column toward the cells of origin of the DSCT in the upper lumbar region (147). After early attempts to identify the segmental collaterals of Ib afferents (see Ref. 278), recent studies, using intracellular horseradish peroxidase labeling of functionally identified afferents, provided detailed information on the distribution and location of Ib terminals in the lumbosacral spinal cord (39,40, 141,147). Reconstruction of the trajectories of 11 fibers originating from either triceps surae or unidentified muscles innervated by the posterior tibia1 nerve was achieved by Brown and Fyffe (40), and a further 5 fibers from soleus, hamstring, and quadriceps muscles were traced by Hongo et al. (147). Over intraspinal axonal lengths of 5-10 mm, each axon gave 5-11 collateral branches at intervals of lOO2,600 pm. The collaterals ran ventrally in the dorsal horn toward their terminal arborizations in laminae V, VI, and VII (see Fig 12.9 in Ref. 39). Each terminal arborization gave 56-384 synaptic boutons, mainly of the en passant type (40). In the upper lumbar segments, extensive terminal branching was seen within Clarke’s column, but some terminals went further ventrally to end in laminae VII and VIII. Afferents from thigh muscles had more terminal arborizations outside Clarke’s column than afferents from shank muscles, suggesting a somatotopic organization of Ib fiber terminations (147). The location of Ib terminals in lumbar cord shows good correlation with the sites of Ib synaptic connections (see sect. VII@. D. Development of Tendon Organs

Data on the development of mammalian tendon organs were provided by the study of Zelena and Soukup (314, 343) carried out in rats (see also Ref. 328). They showed that tendon organs begin to differentiate at a late stage of fetal development. In the leg muscles of rat fetuses, nerve branches appear near the boundaries between muscles and aponeuroses before 18 days of gestation, and 3 days later, discrete islets are seen bulging from the aponeurosis toward the muscle. These islets contain thin collagen bundles and the tips of myotubes starting to form myotendinous junctions. A single nerve fiber enters this area and branches to give terminals near or in contact with myotubes. At birth, the innervated core of the differentiating tendon organ becomes elongated due to proliferation of Schwann cells and fibroblasts interposed between the aponeurosis and the myotube tips. Collagen bundles assemble between Schwann cells and nerve terminals, which continue to ramify. The capsule is formed by day 2 after birth, enclosing the body of the tendon organ. A fascicle of five to nine muscle fibers enters the capsule,


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establishing myotendinous junctions at variable distances from the aponeurosis. During the subsequent growth of the tendon organ body, the muscle fibers attached to the collagen bundles gradually recede from the capsule and lose their nerve terminal contacts. From 5 days postnatal onward, nerve terminals are only found among collagen bundles. By day 7 postnatal, muscle fibers have left the intracapsular lumen; their connection to the aponeurosis is by tendinous fascicles, which also interconnect with the collagen bundles assembled around the nerve terminals. In the course of the second and third postnatal weeks, septal cells appear to divide the intracapsular space. The myelination of the Ib fiber occurs postnatally. After 3 wk postnatal, the tendon organ has acquired its main structure, and subsequent growth only concerns its length. Records of muscle receptor discharges were obtained in kittens, suggesting that some tendon organs can signal contraction as early as 2 days postnatal (124). III.

DISTRIBUTION

A. Numbers

of Tendon Organs in Various

Muscles

In cats, the exact numbers of receptors are known for only 10 hindlimb muscles and a few others, as listed in Table 1. In other species, muscle receptors were counted in the mouse gastrocnemius medialis [5-7 tendon organs per muscle (341)], and for some intrinsic hand muscles of the bonnet monkey (Macaca radiata), there are data collected by Devanandan et al. (73). In small muscles, the tendon organ content displays TABLE

1. Numbers

of tendon organs and spindles found

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considerable variability. For instance, the populations of the five cat peroneus tertius muscles examined by Scott and Young (306) varied in a range of 7-15, with a mean number of 10 tendon organs per muscle. The spindle population of these muscles was larger and less variable. Hand muscles of the bonnet monkey provide further instances of variability in tendon organ content. There are, on average, 7 tendon organs in abductor pollicis, in a range of 1-15, and 5 in the first dorsal interosseous, in a range of l-9. Moreover, tendon organs can be lacking in lumbrical muscles (means 0.16 and 0.28, respectively, for the first and second lumbrical) and in the abductor digiti minimi (mean 2.5, range O-7), whereas spindles are always present in larger numbers and with less variability than tendon organs (73). A similar lack of tendon organs was reported for the spindlerich lumbrical muscles of the marsupial phalanger forepaw, which has prehensile capabilities (190). The functional significance of such paucity in tendon organs is not understood. Hand muscles perform very fine and precise movements with accurate force gradation, and the fact that some of them are deprived of tendon organs would suggest that information provided to the central nervous system by other receptors (muscle, joint, or skin receptors) can compensate for the absence of input from tendon organs. There is an obvious need for further data on the receptor content of hand muscles in primates and other species. B. Ratios of Motor

Units to Tendon Organs

The proprioceptive equipment of a muscle is usually quantified in terms of density (i.e., the number of recepin diferent

cat muscles

Numbers

Hindlimb

muscles

Semitendinosus Rectus anterior femoris Soleus Medial gastrocnemius Flexor digitorum longus Peroneus tertius Peroneus brevis Peroneus longus Extensor digitorum brevis 5th interosseus

86” ‘78” 45” 44” l7a 36” 16” 35” 25”

137” 102” 53” 70” 51” 14” 40” 17” 56” 27”

Flexor carpi radialis Intercostalis 4th internus and externus Temporalis Masseter Dorsolateral tail

308

60g

0.50

17” 2oh 6h 53’

49” 74h 34h 63’

0.34 0.27 0.17 0.84

10”

255b

Other

0.62 0.76 0.85 0.62 0.33 0.71 0.90 0.94 0.62 0.92

3

1.9

3.3 5.8

2.8 3.6 3 2.5 1.7 5.7 2

9.1 3.5

1.9 6 3.3

muscles

Number of motor units comprising the muscle given when known. a From Ref. 16. b From Ref. 34. Ref. 53. e From Ref. 306. f From Ref. 153. g From Ref. 281. h From Ref. 212. i From Ref. 107.

’ From Ref. 89.

d From


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tors per gram of wet muscle weight) rather than by the total number of receptors in the muscle. However, because tendon organs are muscle contraction sensors, the ratio of motor units to tendon organs might be a functionally more significant number than the receptor density. Table 1 shows the range (1.9-9.1) of the ratios obtained for eight muscles in which both tendon organ and motor unit populations are known. As a tendon organ can signal the contraction of a single motor unit (156), a low ratio indicates the possibility of a close monitoring of motor unit contraction by each receptor. Table 1 also shows the ratios of motor units to spindles, as earlier proposed by Cooper (64). All the muscles have lower ratios for spindles than for tendon organs, but in some muscles, such as the peroneus brevis and longus, the differences are slight.

gaged in dyads, often with partial fusion of spindle and tendon organ capsules (212). Another receptor frequently associated with the tendon organ is the paciniform corpuscle, as already mentioned in early descriptions by Cattaneo (56) and by Ruffini (294, 296). Paciniform corpuscles resemble miniature Pacinian corpuscles, are -180 pm long and 20 pm wide, and are innervated by fibers of 3-12 pm in diameter, which means that the larger ones may fall within the group I range (317; Pang in Ref. 17). In the sample studied by Stacey (316), 15% of 158 tendon organs were associated with paciniform corpuscles, located either on the surface of the tendon organ or within its capsule. The functional significance of tendon organ associations with either spindles or paciniform corpuscles remains so far unknown.

C. Ratios of Tendon Organs to Spindles

IV.

With rare exceptions (see Ref. 16), cat muscles contain more spindles than tendon organs (Table 1). This is also the case for the mouse medial gastrocnemius in which Wohlfart and Henriksson (341) found a ratio of 0.58, with 7 tendon organs and 12 spindles. However, in some cat hindlimb and tail muscles, the ratio is close to 1, whereas in contrast jaw muscles have particularly low ratios of 0.27 for temporalis and 0.17 for masseter (212). Again, the relative paucity of tendon organs in jaw muscles has to be kept in mind when considering the fact that the contraction of these muscles determines the biting force, i.e., a precisely controlled parameter of motor acts involved in eating, hunting, and fighting. The functional significance of the tendon organ-to-spindle ratio is not known (226). At any rate, the ratio does not seem related to the size of the receptor population in the muscle, since, for instance, the receptor-rich peroneus brevis and the receptor-poor peroneus longus have similarly high ratios of tendon organs to spindles.

The contraction of muscle fibers attached in series with a tendon organ provides the specific stimulus for the receptor because it strains the collagenous bundle, which entails deformation of sensory terminals, producing conductance changes in their membrane. A receptor potential thus arises and spreads to an impulse initiating site where the action potential is generated. In outline, “sensory transduction” processes in tendon organs can be divided into three steps: 1) a mechanical step, in which the force developed by muscle contraction is transmitted to the sensory terminals; 2) the transduction step proper, in which deformation of terminal membrane leads to the occurrence of a receptor potential; and 3) an encoding step, in which the information contained in the shape of the receptor potential (i.e., slope, amplitude, and time course) is transformed into a discharge frequency. The structural features of tendon organs inspired hypotheses about the mechanical step of transduction (35,326,344). The braiding of unmyelinated sensory terminals with collagen filaments in the neurotendinous compartment does suggest that stretching of collagen bundles will cause lateral compression or/and longitudinal extension of the terminals. Deformation is probably not restricted to the portions of terminal membrane actually pulled on or pinched by collagen fibers; distension of membrane may also occur in other axonal ramifications when they receive the volume of axoplasm squeezed out from the compressed terminals. Most of our knowledge about transduction in tendon organs comes from studies of receptors isolated in vitro from cat dorsolateral tail muscles (99-101, 338). These thin muscles (164, 166), containing numerous spindles and tendon organs (107; Table 1), comprise but a few layers of muscle fibers so that a gentle lateral pull on their longitudinal tendon makes muscle receptors visible under the dissecting microscope. By delicate dissection, a tendon organ can be removed from the muscletendon junction, together with its innervating Ib fiber (and, in some instances, in-series muscle fibers) and

D. Association of Tendon Organs With Other Receptors

An intriguing feature of tendon organ distribution is their relatively frequent association with spindles. Occasionally, the tip of an intrafusal muscle fiber attaches in series with a tendon organ (17,18,107), which makes theoretically possible the activation of the tendon organ by specific fusimotor axons, but such an instance has never been reported. Much more frequent is the in-parallel association of tendon organ and spindle called “dyad” (225). In some muscles of the cat leg (soleus, medial gastrocnemius, and extensor digitorum brevis), ZO-50% of tendon organs were found in dyad association with spindles (225), whereas in others (peroneal muscles) the proportion was ~10% (306). Dyads were also reported to occur in flexor carpi radialis (281), in tail muscles (107), and, again with a high incidence, in neck muscles (279). A particularly striking case is that of iaw muscles in which all the tendon organs are en-

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transferred into a bath of physiological solution covered with mineral oil. A portion of the nerve fiber is raised to a microelectrode placed in the oil layer for recording of either action potentials or receptor potentials after blockade of impulse initiation by tetrodotoxin. The muscle end of the isolated tendon organ is tied to a stretching device producing either sinusoidal or rampand-hold stretches. Controlled length changes applied by this means provide efficient mechanical stimulation of the preparation. The tendon end of the receptor is tied to a miniature strain gauge force transducer, allowing measurement of the forces developed in response to the imposed stretches. Most of the experiments with isolated tendon organs were carried out at a temperature of %“C, and the preparations were found to maintain their responsiveness to stretch for several hours. It is difficult to assess the effects of this temperature (the temperature of cat tail muscles is usually -34°C) or of the absence of blood supply on the studied receptors. The possibility that tendon organs in situ display slightly different features should not minimize the value of the data obtained with in vitro studies because there is no other way of gaining insight into the different steps of transduction. A. Mechanical Properties of Tendon Organs: Stress and Strain

Deformation caused by length changes applied to the muscle end of an isolated tendon organ is transmitted to the sensory endings essentially through the collagen bundles (but also through the capsule walls, septa, and other intracapsular structures surrounding the sensory terminals). The amplitude and time course of force variations recorded at the tendon end of the receptor are therefore likely to reflect the characteristics of the longitudinal forces actually sensed by the terminals. This is a basic assumption in the interpretation of observations made on isolated tendon organs. In a sample of 11 isolated tendon organs (lOl), the relation between imposed changes in length (or strain) and force developed per unit of cross-sectional area (or stress) measured during the hold phase of ramp-andhold stretches, that is, under static conditions, was approximately linear. Strain was kept 20 Hz, and, at all the tested frequencies, the gain declined for stretch amplitudes beyond the linear range. This suggests that the dynamic sensitivity of receptor potentials in tendon organs is not a simple sensitivity to velocity because, during sinusoidal stretch at a constant frequency, increase in amplitude necessarily implies faster velocity, and a sensitivity to this parameter would therefore be expected to cause an increase in gain. However, in other mechanoreceptors, such as spindle primary endings, known to display a very high dynamic sensitivity, reduction in gain of receptor potential also occurs when amplitude of sinusoidal stretching is extended beyond the linear range (167). The dynamic sensitivity of the receptor potentials of tendon organs in vitro was similar to that of spindle secondary endings in the same condition and considerably less than that of primary endings. The authors considered the possibility

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that their experimental conditions were responsible for the relatively low dynamic sensitivity of isolated tendon organs, because in other in situ studies higher values were reported (9,288). However, these studies dealt with tendon organ discharges in a restricted range of conditions (see sect. VA) and not with receptor potentials. As is seen in the next section, the impulse inititiating mechanisms of tendon organs have a dynamic sensitivity of their own that comes in addition to the dynamic sensitivity of receptor potentials. C. Impulse Initiation

The location of the impulse initiating site of tendon organs is not known. Neither is it known whether the receptor has a single or several such sites. The neural compartment of the capsule contains myelinated nerve fibers that are first- and second-order branches of the innervating Ib axon. Whereas unmyelinated sensory terminals are thought to generate only receptor potentials, myelinated fibers are considered to conduct action potentials, and, theoretically, initiation of impulses could be expected to occur near any point of continuity between unmyelinated terminal membrane and myelinated axonal branch, usually at the first node. However, this is not obligatory, since in some frog muscle spindles, impulses are generated at one terminal node and not at the others (172). Another possibility could be considered, that in tendon organs electrotonic propagation of receptor potentials occurs in the myelinated branches of the Ib axon, transmitting information from all the terminals up to a single site of integration and impulse initiation (100). The assumption that the discharge issued by a tendon organ results from the interaction of several sites of impulse initiation is attractive, however, because such interactions could help to explain some observations on the nonlinear summation of tendon organ responses to different stimulations. Proske (273) clearly pointed to the speculative character of the evidence in support of this assumption, which is further discussed at the end of this section. Fukami (100) measured the absolute force threshold for discharge of an action potential by an isolated tendon organ during the contraction of in-series muscle fibers using a preparation in which the muscle fibers inserting on the isolated tendon organ were dissected along their total length. The effects of varying muscle length on the force developed and on the response of the receptor could thus be tested, and threshold measurements were made at the length for which the force of a twitch contraction was maximal. Absolute force thresholds, including both active and passive components, ranged between 4.5 and 22 mg, and, in the same preparations, the peaks of twitch contractions elicited in single in-series muscle fibers were in a range of 2-20 mg. The contraction of a single in-series fiber may, therefore, suffice to elicit a discharge from a tendon organ. In fact, in Fukami’s sample, 8 of 15 isolated tendon organs were sensitive enough to discharge an action potential in response to the twitch of a single in-series fiber.


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In three preparations, the threshold force for eliciting a sustained impulse discharge (lasting for 3-4 s) from an isolated tendon organ during the hold phase of an applied stretch could be measured directly by Fukami and Wilkinson (101). Threshold values of 10, 50, and 170 dyn, respectively, were found for the three tendon organs, and beyond this threshold, discharge frequencies increased linearly with force. The extent of the range over which linearity prevailed is not clear because, although the authors stated that “the discharge frequency is approximately proportional to applied tension over a wide range,” their illustrated example (see Fig. 1 in Ref. 101) displays a decrease in the slope of the discharge frequency-tension relation for tensions higher than -60 mg. In preparations where isolated tendon organs could be activated by the contraction of in-series muscle fibers (loo), the relation of discharge frequency to plateau tension (elicited by direct stimulation of the muscle fibers at rates of 25-40/s during 1.5-Z s) also showed a limited linear range of ~100 mg, beyond which the slope of the relation declined. Given the nonlinearities of the first two steps of transduction, it would have been a surprise if linearity had been restored through the encoding step. As mentioned, a comparison of the mechanical properties of isolated tendon organs with the static sensitivity to stress of their discharge revealed an important feature, namely, that the more compliant receptors had the higher sensitivities. The functional importance of this point has already been emphasized. Sensitivities of isolated tendon organ discharges to the force developed by tetanic contractions of in-series muscle fibers were measured in five preparations and found to range between 99 and 335 impulses s-l g force-’ (100). Variations in the length of the preparation left the sensitivity of the tendon organ practically constant up to the length at which the force developed by a twitch contraction was maximal. Extension beyond this length caused an appreciable reduction in sensitivity, possibly due to a reduction in compliance of the tendon organ. This loss of sensitivity of the discharge, however, appears contradictory with a later observation of Wilkinson and Fukami (338) in which an increased stiffness of isolated tendon organs, obtained by extending their initial length, resulted in augmentations of sensitivity to sinusoidal stretch of both tension responses and receptor potentials (see sect. IV, A and B). Accomodation at the impulse initiating site might account for the specific dynamic sensitivity of impulse initiation in tendon organs. Records of action potential discharges superimposed on receptor potentials during ramp stretches at increasing velocities clearly demonstrated that with the faster length changes, eliciting steeper slopes of receptor potentials, the threshold for impulse initation was lower than with slow ramps (see Fig. 3 in Ref. 101). This strongly suggests the occurrence of accommodative processes in impulse initiation that are possibly responsible for the adaptation of the discharge on application of a steady stimulus. The dynamic sensitivity of tendon organ discharges l

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in response to sinusoidal stimuli has not been examined in vitro, but observations made in vivo on the responses of tendon organs to unfused contractions of single inseries motor units provided relevant data on this point (179), as discussed in section vCS. Some individual Ib axons innervating cat tail muscles divide to supply two different tendon organs. Fukami (99) was able to separately stimulate each receptor in such pairs and to record the discharges from their common axon. This situation afforded a unique opportunity of observing the interactions of action potentials originating from two distinct initiating sites. In the first place, the emission of an impulse by one of the tendon organs was found to cause a reduction of excitability, lasting 80-200 ms, in the second receptor. This is probably because on arrival at the branching point the impulse propagates both orthodromically into the parent Ib axon and antidromically into the branch supplying the “partner” tendon organ. It is not known whether antidromic invasion proceeds back to the terminal membrane or only to the impulse initiating site of the partner, but it certainly influences the activity of the second receptor. When one of the tendon organs is steadily discharging, the emission of a single action potential by the partner tendon organ during an interval of the discharge causes “resetting” (227) of the discharging receptor, which lengthens the delay of occurrence of the subsequent impulse. When both tendon organs in a pair are activated, three types of interactions may occur between their impulses, depending on their discharge frequency: I) if both discharges have low frequencies, with interimpulse intervals longer than the period of reduced excitability in each tendon organ, then pure summation may occur, with impulses from both receptors appearing in the resultant discharge of the parent axon; 2) when the discharge rates are very different, high-frequency impulses emitted by one of the partners will reset the second one, which can result in total suppression of the slower activity so that the parent Ib axon will only transmit the high-frequency discharge; and 3) finally, discharges at similar intermediate frequencies can be expected to mix, following a probabilistic process, in the parent axon. Returning to the problem of multiple sites of impulse initiation in tendon organs, there is so far no direct evidence in support of this assumption. If several generators of action potentials were present in a tendon organ, their patterns of interactions would reproduce those observed in pairs of receptors innervated by a single Ib axon. Effects observed in single tendon organs on combination of two different stimuli rarely suggest a simple summation, as in the experiment of Fukami (loo), who applied a constant depolarizing current to an isolated tendon organ and simultaneously elicited the contraction of in-series muscle fibers. Each stimulus on its own evoked a discharge, and the response obtained with a combination of both stimuli merely suggested that summation of receptor potentials occurred at a single impulse initiating site (but another possible interpretation could be that summation of low-frequency


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discharges generated at two sites occurred in the axon). In experiments in vivo, stimulation of tendon organs by combined contractions of several motor units usually produces nonlinear summations of responses that do not easily lend themselves to diagnosis of multiple sites of impulse initiation or pacemakers because nonlinearity is a very common feature in the different steps of transduction in tendon organs. There is, however, an observation reported by Gregory and Proske (122) for which the existence of separate pacemakers would readily provide an explanation. When a tendon organ was activated at short interval by two successive tetani of a single in-series motor unit, the dynamic peak present at the onset of the first response was absent from the second response. This disappearance of the dynamic peak was considered to represent some “adaptation” phenomenon. When the response of the tendon organ to the same motor unit was elicited after activation of the receptor by another inseries motor unit, the second response had a dynamic peak. Adaptation did not occur when the tendon organ was activated by two different motor units in succession. The lack of adaptation between the responses to different motor units was interpreted by the authors in terms of multiple sites of impulse initiation. If each unit elicited a discharge from a different pacemaker, activation of one pacemaker did not entail adaptation at the other pacemaker, hence the persistence of the dynamic peak. Computer modeling was used by Gregory et al. (120) to test this hypothesis on the responses of soleus tendon organs to combined stimulation of ventral roots. The observations were found compatible with the presence of multiple impulse initiating sites. However attractive, this explanation can only be considered tentative until the multiplicity of pacemakers in tendon organs is actually demonstrated (see Ref. 273). In conclusion, the functionally significant features at each step of sensory transduction in tendon organs could be summarized as follows. I) The mechanical step consists of deformation of the receptor by the applied force. The stress-strain relation is approximately linear under static conditions (but not under dynamic conditions), with large differences in slope, depending on variations of stiffness among individual tendon organs. Stiffness is a major factor of tendon organ sensitivity. Z) The amplitude of the receptor potential is linearly related to the applied force under static conditions, but nonlinearity prevails under dynamic conditions. The dynamic sensitivity is likely to depend on ionic mechanisms, since it is virtually absent from the mechanical step. 3) The threshold contractile force for the discharge of an impulse is 1,000 g). Moreover, about one-quarter of the receptors did not give a maintained discharge when the muscle was stretched up to its physiological limit, and one-half of these did not respond at all even when the muscle was overstretched beyond this limit, whereas they displayed a fairly low threshold for twitches. Later on, Houk and Henneman (156) also pointed out that very few of the soleus tendon organs they studied did discharge steadily for stretches less than the maximal physiological length of the muscle. A controversy about the sensitivity of tendon organs to stretch started after the observations made by Alnaes (3) in another muscle, tibialis anterior. In that sample of 22 tendon organs, all responded to passive stretching of the muscle within physiological limits, most had similar thresholds for twitch and passive ex-

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tension, and four receptors even discharged spontaneously in the absence of muscle stretch. The difference of behavior between soleus and tibialis anterior tendon organs was ascribed to differences in muscle internal mechanics. A further investigation, in soleus again, by Stuart et al. (322) brought the conclusion that the sensitivity of tend .on organs to passive muscle stretch, as may occur during normal changes of posture and locomo tion, was sufficient to elicit a significant Ib input to the central nervous system during such activities. A notable particular of their experiments is the fact that, taking into account the dynamic sensitivity of tendon organs, the authors examined the responses of the receptors to stretches applied at velocities comparable to the rate of active tension changes occurring during contraction. In a subsequent study, however, the same group clearly showed that tendon organs had lower thresholds for active than for passive force, since the ratios of passive to active force thresholds of individual receptors varied in a range of 0.3-230 for soleus and of 0.2-40 for tibialis anterior tendon organs (see Figs. 9 and 10 in Ref. 323). In both samples a single receptor was at the lower end of the range, with a ratio (3. Finally, Stephens et al. (321) concluded that passively developed force is a relatively ineffective stimulus for the excitation of tendon organs. The poor performance of tendon organs as passive tension sensors was conclusively demonstrated by Houk et al. (161). In a study carried out on three different muscles of the cat hindlimb, they examined 32 tendon organs from soleus, 19 from medial gastrocnemius, and 79 from tibialis anterior. These experiments were made on muscles with intact origins and insertions, which allowed accurate determination of the maximal physiological length of the muscle in situ. The full range of normal muscle lengths was explored with passive muscle stretch applied by flexion or extension of the ankle joint through its full normal range. For each receptor, the degree of “static” muscle stretch eliciting a discharge was measured, taking into account only the discharges that were maintained for 1 min after completion of the length change in the absence of any contraction. An actual “stretch receptor” would be expected to meet this criterion. In the whole sample, only three tendon organs (one from medial gastrocnemius and two from tibialis anterior) had a spontaneous discharge at the minimal muscle length, but their discharge frequency did not increase with further stretch, except when the muscle length reached physiological limits. The proportion of tendon organs that had a steady discharge within the physiological range of muscle lengths did not exceed 35%, but again these receptors did not increase their discharge frequency on further muscle extension, as would be expected if they were to signal muscle stretch. Another 17% could be made to produce a steady discharge only when hyperextension or hyperflexion of the ankle joint brought the muscle beyond the physiological range of length, and the remaining 48% did not respond at all whatever the muscle length. Altogether, of this relatively large sample of tendon organs, 65% could simply not fu nction as detectors of ‘‘excessive” muscle ten-


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sion because their threshold was higher than the maximal passive tension developed at the maximal possible length of the muscle. This conclusion was confirmed by also testing the “phasic” responses of tendon organs to rapid passive stretch. Tendon organs of intact tibialis anterior muscles were examined during rapid (130-160 mm/s) ankle extensions elicited by stimulating at 40/s during 1 s the cut nerve to triceps surae with supramaximal strength. In a sample of 54 receptors, only 21 responded with A0 impulses to the brief extension of their muscle produced by contraction of the antagonist, whereas another 13 tendon organs gave a short burst of ~10 impulses (see also Fig. 1 in Ref. 280), and the remaining 20 (37%) gave no response at all. The short phasic bursts produced by some tendon organs on rapid passive stretch have been used to elicit Ib afferent volleys in studies on central actions of tendon organ afferents (e.g., see Refs. 97,222). The proportion of receptors giving a phasic response to a rapid stretch was higher than the proportion responding to maintained muscle extension (see also Refs. 322, 323), but still more than one-third of the examined tendon organs were not activated by fast passive muscle lengthening. The phasic responses of tendon organs point to the dynamic sensitivity of these receptors, i.e., a sensitivity to the rate of tension change. This property was recognized in early studies (3,156,187,228), but it is generally not considered functionally significant, and, in handbooks, tendon organs are often presented as receptors with a low dynamic sensitivity (e.g., see Ref. 135). The bases for this statement require reconsideration because they were provided by investigations in which muscle stretch was used as a stimulus (e.g., see Refs. 112, 159). First, it is not surprising to find a low responsiveness of tendon organs to longitudinal vibration of the passive muscle, especially when tendon organs are compared with spindle primary endings (41), since passive muscle stretch is an adequate stimulus for the latter but not for the former receptors. Second, the responses of tendon organs to ramp profiles of active force were examined by Stauffer and Stephens (320), who concluded that the dynamic responses of the receptors did not represent an indication of the rate of force change recorded at the tendon. However, their observations were made on ramp force profiles produced by stretching the contracting muscle with a servo-regulated muscle puller arranged in force servo so that in fact they examined the dynamic responses of tendon organs to muscle stretch, i.e., again not to their specific stimulus. Finally, most of the mathematical models that have been derived from tendon organ responses to sinusoidal muscle stretches (9,159,196,282,288) describe the behavior of the receptor within a narrow range of restrictive conditions, such as linearity and invariance in time, that are not permanently prevailing under natural circumstances. In summary, the dynamic properties of tendon organs are not fully displayed when the receptors are activated by nonadequate stimuli, but, as is discussed in section vC5, it does not follow that the dynamic sensitivity of tendon

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organs is also negligible in responses to specific stimuli, i.e., contraction of in-series motor units. Returning to the designation of tendon organs as stretch receptors, it is clear that isolated tendon organs do respond to stretch applied at one of their ends (see sect. IV). Why, then, do they appear relatively insensitive to stretch of the whole muscle when tested in situ? This is because the tendon organ, placed in series with a fascicle of muscle fibers, is in parallel with most of the connective tissue within and around the muscle (154, 156). The stiffness of the connective component is responsible for much of the passive force developed by a muscle when resisting stretch (161), but the tendon organ is weakly affected by this force, which pulls in parallel and not in series with the receptor. In addition, the properties of muscle, tendon, and aponeuroses in series with the tendon organ also act as “mechanical filters” distorting the transmission to the receptor of mechanical inputs applied at the muscle end (154). In conclusion, even though the intrinsic properties of tendon organs would allow them to work as stretch receptors, their functional properties, as determined by their location in muscle, do not include a significant sensitivity to passive muscle stretch. Tendon organs are more responsive to stretch in a contracting muscle, but even so, their performance as stretch receptors appears dubious because muscle extension does not entail systematic increases in their discharge frequency (e.g., see Ref. 321). B. Speciific Stimulus: Muscle Fibers

Contraction

of In-Series

If consistent responses and low threshold are accepted for criteria, muscle contraction appears as the adequate stimulus for a tendon organ and, more precisely, the contraction of those motor units contributing fibers to the fascicle attached in series with the receptor. This idea gradually gained acceptance after Houk and Henneman (156) demonstrated that individual tendon organs of the cat soleus muscle can signal the activity of single motor units. From their observations, they further inferred that the contraction of one or two inseries muscle fibers should suffice to elicit the discharge of the receptor, an assumption that was later confirmed by studies on isolated tendon organs in vitro (100; see sect. IV). More recently, Spielmann and Stauffer (315), using the glycogen-depletion method (86) to label the muscle fibers of single soleus motor units acting on a given tendon organ in vivo, found that each of these units had one or two fibers attached to the receptor (see also Ref. 118 for similar observations in medial gastrocnemius muscle). Houk and Henneman (156) also demonstrated that a single tendon organ is in series with several motor units, which constitutes the equivalent of a “receptive field.” They found an average number of 10 motor units (in a range of 4-15) acting on individual soleus tendon organs (see also Refs. 28,323) and noted that these numbers represented minimal estimates, since the number


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of muscle fibers in series with a tendon organ can be in a range of 25-50 (see sect. I). Similar sizes of receptive fields were observed in other hindlimb muscles, such as gastrocnemius medialis, tibialis anterior and posterior, and peroneus brevis, longus, and tertius (30, 122, 148, 177,272,323). In peroneal muscles it is not exceptional to find receptive fields of 17-18 units per tendon organ in peroneus longus, 14-15 units in peroneus brevis, and ll12 units in peroneus tertius (unpublished observations from Refs. 148,149,177,179). These numbers represent 18,20, and 35%, respectively, of the motor unit population in peroneus longus, brevis, and tertius (Table 1). The highest percentage corresponds to the smallest muscle, peroneus tertius, possibly because it is relatively easy to examine a large proportion of motor units in a limited population. Alternatively, this high percentage could indicate a particularly tight control exerted by tendon organs on motor unit contractions in small muscles (see Ref. 176). The control appears even tighter when considering the number of tendon organs activated by a single motor unit. Jami and Petit (177) provided evidence that a single motor unit can activate several receptors. In their sample this was the case for 10% of tendon organ-activating units in soleus, 20% in tibialis anterior, 29% in peroneus brevis, and 43% in peroneus longus. Taking into account the size of receptive fields and the ratio of motor unit to tendon organ populations (Table 1), these data strongly suggested that the contraction of every motor unit in a muscle is monitored by at least one tendon organ. Support for this assumption was later obtained in a series of experiments on peroneus tertius in which all the Ib afferent fibers serving the muscle (peroneus tertius contains 10 tendon organs on average; see Table 1 and Ref. 306) could be prepared for recording in dorsal root filaments (152). Randomly chosen samples of six to eight motor units of different physiological types (see sect. VCZ) were tested for their actions on the population of tendon organs, and each unit was found to activate at least one receptor while each receptor was activated by at least one unit. The maximal number of tendon organs activated by a single unit was six, corresponding to more than one-half of the total population in the muscle. Small units of the slow type were found to act on one or two tendon organs each, whereas fast-type units could activate any number of receptors, in a range of one to six, and that number did not appear related to the force developed by the contraction of the unit. It is not known whether in larger muscles single motor units can activate larger samples of tendon organs. C. Activation

of Tendon Organs by Single Motor Units

1. Problems resulting from impossibility of measuring

actual force applied to tendon organ

One basic difficulty in the assessment of the inputoutput relations of tendon organs (i.e., the relations be-

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tween the force actually sensed by the tendon organ on contraction of an in-series motor unit and the discharge frequency of the receptor) is that we have no access to the input (see Refs. 29, 178, 277, 321). A transducer attached to the tendon measures the resultant force produced by all the muscle fibers of the contracting motor unit, whereas the tendon organ is pulled on by one or two muscle fibers (118, 315). Recent data suggest that there are only slight differences between the specific forces of individual muscle fibers belonging to slow- and fast-type motor units (32), but innervation ratios vary among units. Burke and Tsairis (54) counted the fiber populations in motor units of medial gastrocnemius: two units developing similar tetanic forces (35 and 39 g) comprised, respectively, 300 and 500 fibers. If linear addition of individual fiber forces is assumed, the calculated mean force per fiber would be 0.12 g for the smaller unit and 0.07 g for the larger unit. In contrast, the calculated mean force per fiber may be similar in motor units developing different total forces, as in the case of two soleus motor units studied by Burke et al. (50): the first one, comprising 50 fibers, developed a tetanic force of 4.2 g, whereas the second, with a force of 35.2 g, was made of 427 fibers; the mean force per fiber was 0.08 g in both units. A further complication of the relation between the force measured at the tendon and the fraction of this force applied in series with a receptor comes from the location of tendon organs at myoaponeurotic junctions. The orientation of the line of pull of a motor unit with respect to the main axis of the muscle tendon may result in a vectorial loss in the force measured at the tendon (275), which is much less likely to occur for the force sensed by the tendon organ because the receptor is directly pulled on by the contracting in-series muscle fibers. These factors might explain why the force threshold of a given tendon organ is often found to be different for different motor units (177,323). They might also explain, together with other factors (see sect. vE), why the tendon organ sensitivity appears higher for contractile force produced by single motor units (28, 156, 178, 319, 323) than for whole muscle contraction (3, 187). They could further account, again partly, for the difficulty of predicting the response of a tendon organ to the anisometric (i.e., nonisometric but not necessarily isotonic) contraction of an activating motor unit; for two units producing similar activations of the receptor under isometric conditions, muscle shortening does not entail similar modifications of activation, and for two tendon organs activated by the same motor unit, the effects of muscle shortening are not necessarily identical (148). Observations made by Stephens et al. (321) pointed to further discrepancies between force measured at the muscle tendon and force sampled by the tendon organ: when a motor unit acting on a tendon organ was made to contract at different muscle lengths, the optimal length for contractile force was not the length at which the receptor gave a maximal response. Finally, the occurrence of “unloading” (see sect. vE) also provides evi-


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dence that a combination of forces from two motor units can produce different effects on a tendon organ and at the muscle tendon. In conclusion, one can but support the statement by Reinking et al. (277) that the actual sensitivity of a tendon organ cannot be measured in situ; they proposed the operational concept of “apparent sensitivity,” defined as the ratio of the change in receptor discharge frequency to the contractile force measured at the muscle tendon. The absence of a simple relation between the global force and the stimulus that directly acts on the receptor is usually overlooked in tendon organ studies, mostly because the force appearing at the tendon is the functionally significant parameter for posture and movement. 2. Heterogeneity of motor units activating a single tendon organ

In heterogeneous muscles, the receptive field of a given tendon organ, i.e., the set of motor units connected in series with this receptor, includes units belonging to all the physiological types, as defined by Burke et al. (51): slow contracting and fatigue resistant (S), fast contracting and fatigue resistant (FR), or fast contracting and fatigable (FF). Reinking et al. (277) were the first to identify the physiological types of motor units activating individual receptors in medial gastrocnemius muscle. One tendon organ of their sample, for instance, was activated by two S units plus one FF and one FR unit (see also Refs. 122,152,179,272). Among the motor units connected in series with a particular tendon organ, the range of tetanic forces, from -1 to 100 g, is the same as among the total population of motor units in the muscle (see Fig. 3 in Ref. 177; see also Ref. 122). The concept of “sensory partitioning” suggests that muscle mechanoreceptors respond preferentially to events occurring within a limited portion of muscle around each receptor. A special significance is therefore attached to the fact that tendon organs monitor the activity of small sets of motor units located in the same “compartment” (e.g., see Refs. 55,249). This question is not discussed here because it was recently reviewed by Windhorst et al. (340) in a paper accompanied by numerous commentaries from other authors. The contraction of ,&motor units (i.e., units innervated by motor axons supplying both extra- and intrafusal muscle fibers) can elicit tendon organ activation even when the P-unit is stimulated at low rates for which spindle activation is not apparent (93). In contrast, and although intrafusal fibers occasionally insert in series with a tendon organ (18), action of a y-axon on this receptor was, so far, never reported. 3. Responses to twitches of slow- and fast-contracting motor units

A slow-type motor unit often produces weak twitch contractions that may be quite efficient in activating a

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tendon organ provided the unit has one fiber in series with the receptor. A remarkable example of this efficiency was reported by Gregory and Proske (122). In the cat medial gastrocnemius, they found two units, one fast and the other slow, acting on the same tendon organ and developing respective twitch forces of 38 and 0.7 g. The response of the tendon organ to the stronger of the two twitches was a brief discharge of 5 impulses delivered in ~50 ms, whereas the weak unit elicited 19 impulses in -200 ms. The instantaneous frequencies of both discharges were not very different, but, in terms of numbers of impulses, the contraction of the weak unit would have been better signaled to the central nervous system than the contraction of the strong unit. Similar observations with tetanic contractions led Reinking et al. (277) to propose that the apparent sensitivity of tendon organs was inversely related to the strength of the activating motor unit, but other findings did not confirm this relation (see Refs. 30, 178, 319). Whether weak or strong, the twitches of in-series motor units elicit remarkably consistent responses of activated tendon organs. In soleus muscle, Binder et al. (29) found receptors giving nearly identical responses to each of several hundred successive twitches. The consistency of high firing probability under these conditions indicates that the force sensed by the tendon organ during twitches of in-series muscle fibers was well above the receptor threshold for this stimulus (see sect. IvC). In the same experiments, however, slight changes in the slope or amplitude of contractile force, as may result from potentiation or from changes in muscle length, caused changes in the timing and in the number of impulses, which suggests a very high sensitivity of the receptor for small variations in the stimulus. Both observations support the recognition of in-series motor unit contraction as the specific stimulus for tendon organs. 4. Lack of relation between discharge frequency and contractile face in responses to maximal tetani

In a number of studies on tendon organ activation, tetanic contractions were used as a stimulus, because the plateau of a tetanus represents a constant stimulus and elicits steady discharges from the receptor, thus allowing easy quantification of the input-output relation. If tendon organs were encoding contractile force, their discharge frequencies would be expected to display some clear relation with the forces of the contracting units, but this could never be demonstrated. In responses to maximal tetanic contractions, small weak motor units were often observed to elicit higher discharge frequencies than large strong units activating the same tendon organ (28, 122, 156, 178, 277, 319). Moreover, when a given motor unit activates two tendon organs, it may elicit different discharge frequencies (see Fig. 3; see also Refs. 69, 152, 178), and the concurrent contractions of two motor units activating the same receptor produce responses at lower frequencies than would be expected from the addition of the responses to each unit contract-


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ing separately (see sect. vD). These discrepancies are not surprising, given the difficulty of assessing the force actually applied to the tendon organ (see sect. vCI). Other possible causes are discussed in section vG. 5. Dynamic sensitivity of tendon organs, as demonstrated by responses to unfused contractions

Tendon organs usually respond to the isometric tetanus of an in-series motor unit with a “dynamic peak” in the discharge frequency during the rise in force followed by a slow decline to a lower “static” discharge rate maintained during the plateau of the tetanus. During the rise in contractile force, the discharge frequency increases much more rapidly than the input force, which suggests that tendon organs are sensitive to the slope of force development (3, 156, 178, 187, 323). However, responses of tendon organs to tetanic contractions do not allow further display of dynamic sensitivity. Responses to unfused contractions were systematically examined by our group because the common firing rates of a-motoneurons are in a range producing such contractions in the majority of fast-type motor units (136,138). An unexpected outcome of this study was to draw attention on the key role of dynamic sensitivity in tendon organ-encoding processes (179). The force developed in the unfused contractions of a fast-type unit displays rapid oscillations, in phase with the stimulation, superimposed on a steady level. The relative amplitudes of oscillations and steady level depend on the stimulation rate. Low frequencies elicit a series of twitches with almost no steady level, whereas for increasing stimulation rates, the steady level augments while the amplitude of superimposed oscillation declines (see the force records in Figs. 2, 5, and 6). Such force profiles present tendon organs with a complex stimulus comprising static and dynamic components, i.e., the steady level and the oscillations, respectively. In response to unfused motor unit contractions, most receptors were found to discharge one impulse on each force oscillation, that is, on each stimulus, for either constant or variable stimulation rates (148-152, 179). This type of response, illustrated in Figure 2, is termed “1:l driving,” by analogy with certain spindle responses to fusimotor stimulation described by Kuffler et al. (195). Houk and Henneman (156) mentioned its occurrence in tendon organ responses to stimulation of motor units at rates 250 impulses/s), whereas others fire at relatively stable frequencies (see Fig. 4 in Ref. 207). Summarizing diagrams of the behavior of tendon organs in extensor and flexor muscles during a step cycle have been tentatively presented (266,268), but they rest on very small numbers of recorded units and need further confirmation. The statement that some tendon organ discharges include a response to muscle length variations, as recently suggested by records made during paw shakes (269), also requires careful verification. A peculiar feature of tendon organ discharges in natural movements (see Fig. 3) is a steplike increase or decrease in frequency recorded during contractions of increasing or decreasing strength (see Fig. 2 in Ref. 13). Such steps were first observed in humans during graded contractions (see Fig. 1 in Ref. 332; see also Fig. 5 in Ref. 85 and Fig. 8 in Ref. 10) and, following the suggestion of Vallbo (332), have been ascribed to recruitment or derecruitment of motor units in series with the tendon organ. C. Human

Tendon Organs

Microneurographic data demonstrate the usual absence of tendon organ discharge in noncontracting muscles (286,332). In the sample studied by Aniss et al. (lo), six of nine tendon organs from pretibial flexor muscles were silent during quiet standing on a horizontal force platform, and the three discharging receptors had very low firing frequencies, ~10 impulses/s. It was verified that the receptor-bearing muscle was not active, as

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maintenance of this posture essentially depends on the activity of ankle extensor muscles. Interestingly, the proportion of silent tendon organs and the low firing rates of the active ones were similar in a sample of 10 receptors recorded while the subjects were standing on the platform tilted 4” in a direction entailing dorsiflexion and some EMG activity in pretibial flexors. This suggests that the motor units recruited for this activity were not in series with the recorded tendon organs. Evidence for the fact that human tendon organs do not monitor muscle stretch clearly emerges from data obtained in leg (44) and forearm muscles. This negative feature, used by Edin and Vallbo (84,85) as an identifying test, has been systematically investigated by Al-Falahe et al. (2). In their sample, the discharge rate of tendon organs from finger extensor muscles, recorded during pseudosinusoidal movements imposed to the passive muscle, did not display any modulation related to changes in muscle length. In contrast, when the subject was asked to actively reproduce the same movement, the discharge frequency of the receptor was maximal when the muscle shortened. The sensitivity of human tendon organs for muscle contraction is demonstrated by their low thresholds (43, 331) and by consistant observations that their discharges are related to the EMG of the receptor-bearing muscle or to the torque produced by its contraction (2, 43,44,85,331). However, the relation is not simple (e.g., see Fig. 4B in Ref. 85; see also Figs. 5 and 8 in Ref. lo), and it seems appropriate to retain the statement of Vallbo (332), describing the human tendon organ discharge as a discontinuous function of the total muscle force. One striking feature of tendon organ activities recorded in human studies is the low frequency of their discharges. The receptor illustrated by Vallbo (see Fig. 1 in Ref. 332) had a maximal rate of ~30 impulses/s for a relatively weak con traction producing a torque of -0 .15 N m (see also Ref. 84). The tendon organs recorded bY Aniss et al. (10) fired at similarly low frequencies, with occasional peaks at 50 impulses/s during moderate swaying movements of the body. Spindle discharges recorded in the same subjects under similar experimental conditions had comparably low rates (see also Refs. 84, 85, 286). Limited discharge frequencies may be related to the necessary limitation of contractions or movements performed by the subject to preserve the precarious contact of the microelectrode with the recorded afferent fiber. In conclusion, both animal and human data support the idea that tendon organs monitor muscle contraction and not muscle stretch. During normal voluntary contractions, the messages from tendon organs to the central nervous system contain at least the information that motor units are activated, i.e., that motor commands are being executed. This is a conservative statement, since for the moment the relationship between contractile force and receptor discharge frequency under conditions of natural contractions remains to be determined. l


July 1992 VII.

CENTRAL

GOLGI

ACTIONS

OF TENDON

TENDON

ORGANS

An obvious function for contraction monitors would be to feed back information about muscle activity to the central nervous system, first to the spinal cord, because reflex regulation of motor output might be easier if assisted by a feedback control of force, and also to upper levels, because precise movements require intentional force adjustments. Assessment of contractile force from tendon organ discharges, as recorded under experimental conditions, is problematic (see sects. v and VI), but the processing of naturally occurring discharges might ’ allow the central nervous system to extract the relevant information. How this would be carried out is far from being understood. Command of muscle contraction can be either reflex, automatic, or voluntary, and most movements involve a blend of the three types of command. The use of feedback from muscle afferents is likely to be different in each blend, as also may be the perception of contractile force. At any rate, these concepts cannot be discussed without a previous analysis of the neuronal networks, essentially located in the spinal cord, in which impulses from tendon organs are dealt with. The most extensively studied spinal system so far is the cat lumbar complex where afferent information from hindlimbs is processed. Work on actions of forelimb afferent input in cervical segments started more recently, and we have much less data on the effects of tendon organs there (see Refs. 5-7, 15). The targets of Ib afferent fibers in the lumbar spinal cord are interneurons and cells of origin of spinocerebellar tracts. After a brief recall of historical background (see Refs. 238, 229, 272), a summary of the available data is presented. Studies on force feedback and perception are considered later. A. Methodological Problems Related to the Diflculty of Selectively Activating lb Fibers

The muscle contractions that excite tendon organs under natural conditions are usually unfused, partial, and not necessarily isometric. This kind of stimulus acts not only on tendon organs but also on other types of mechanoreceptors, both within and without the muscle. Small intramuscular length changes due to interactions between contracting and noncontracting muscle portions will excite spindle primary and secondary endings, and contraction may also activate some nonspecific receptors as mentioned (see sect. VG and references cited there) while joint and skin receptors are pulled on or strained. Whatever the experimental conditions, it is impossible to elicit a pure Ib afferent input by natural stimulation of tendon organs. Under the more usual experimental conditions, electrical stimulation of afferent fibers in cut muscle nerves is employed to elicit synchronous volleys of afferent impulses. Given the distribution of conduction velocities among afferent fibers (see sect. II@ and the correlation of conduction velocitv with diameter and ex-

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citability threshold, a fine gradation of stimulus strengths should allow an orderly recruitment of fibers. However, a strict segregation of afferent fibers on the basis of electrical thresholds remains a theoretical possibility rather than a reliable procedure. The problems of selective stimulation of functionally defined afferent fibers have been fully discussed, and the available solutions have been reviewed by Matthews (229), McIntyre (238), Jack (173), and Proske (272). Within group I, the thresholds of spindle and tendon organ afferent fibers are very close and on the average lower for the most excitable Ia fibers than for the most excitable Ib fibers. For stimulation strengths above group I threshold, the relative proportion of Ia and Ib fibers recruited may vary among muscle nerves. In the cat semitendinosus nerve, a stimulus recruiting 50% of the Ia fiber population is unlikely to engage any Ib fiber, whereas in medial gastrocnemius and peroneus longus nerves, the same stimulus may recruit 15-20 and 40%, respectively, of the Ib fiber complement (66,175,200,324). However, in none of the commonly used muscle nerves is there a significant proportion of Ib fibers that might be recruited by a stimulus below threshold for Ia fibers. For practical purposes, it is accepted that a stimulus strength of up to 1.3 times the group I threshold engages almost exclusively Ia fibers. A usual procedure is to examine whether further increases in stimulus strength entail modifications of the observed effect. Qualitative changes, such as the superimposition of an inhibitory effect on a previous excitatory effect, occurring when the stimulus is increased within the group I range (up to 1.8 times threshold) are ascribed to Ib fibers or “highthreshold group I muscle afferents.” Of course, the rise in stimulus strength is also increasing the number of Ia fibers recruited, but evidence has not been provided so far that this increase might produce a qualitative change in the observed effect. The diagnosis of Ib effects is considered safe, therefore, if these effects are obtained with stimuli maximal for group I and if no further qualitative change appears when stimulus strength exceeds the group II threshold. Methods for selective stimulation of Ib fibers require special procedures and preparations in which the nerve is left in continuity with the receptor-bearing muscle. One method, proposed by Lundberg and Winsbury (222), rests on the fact that tendon organs become more responsive to stretch during muscle contraction. With the muscle initially slack, a brief pull applied during the rising phase of a twitch can elicit an extra impulse in the responses of tendon organs to contraction. It was thus found possible to produce synchronous afferent volleys engaging ~75% of the Ib fiber population superimposed on the background of relatively weak (because the muscle was slack) responses to contraction. The basis of the second method (67, 173) is the observation that prolonged activation of muscle spindles at high frequency induces a decrease in the electrical excitability of their afferent fibers in the muscle nerve. Small-amplitude (-100 pm peak to peak) longitudinal vibrations at 200 Hz. applied to a muscle tendon. can


648

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drive at the same frequency the discharges of most spindles in this muscle (but not of tendon organs; see Ref. 41), and after -20 min of such vibrations, the electrical threshold of the Ia fibers rises above that of Ib fibers for d-15 min. A weak electrical stimulation (usually 1% 1.3 times group I threshold) applied to the muscle nerve during this period will recruit only Ib fibers. This method has proven useful in studies of Ib central projections and actions (e.g., see Refs. 22, 38, 97, 111, 240). With recent advances of studies in spinal pathways, additional tests for the identification of central Ib actions became available. The discriminative value of these tests rests on their association. For instance, interneurons mediating “nonreciprocal” inhibition (see sect. VIIB3) can be recognized by the conjunction of three criteria: 1) they are excited by group I afferents, 2) they are located in laminae V-VI of lower lumbar segments, and 3) they send a collateral projection to Clarke’s nucleus where they exert an inhibitory action on cells of the DSCT (145,146). Of course, the additional operations necessary for establishing all the criteria do not simplify the experimental procedures, but there is for the moment no other way of ascertaining which afferent’s effects are being investigated. A fairly certain correlation between activity in Ib afferent fibers and effects recorded in motoneurons was established by Watt et al. (337) using the method of spike-triggered averaging (244). This method involves a number of technical difficulties, including the functional isolation of afferent fibers in dorsal root filaments maintained in continuity with the spinal cord. After isolation of a filament containing a fiber connected to a discharging tendon organ, a microelectrode is inserted in a motoneuron. Averaging of intracellularly recorded membrane potential is then triggered by the occurrence of impulses in the dorsal filament. Several thousand sweeps must be averaged to allow extraction of significant events from the noise, and a rigorous scrutiny has to be exerted to exclude averaging of artifacts. Unitary postsynaptic potentials related to incoming Ib impulses were thus demonstrated in motoneurons. The projections of 21 Ib fibers from medial gastrocnemius muscle were found to elicit postsynaptic potentials in 86 motoneurons of different species. The potentials were mostly inhibitory (see sect. VIIB~) in homonymous and synergist motoneurons, with amplitudes in a range of 1.4-16.9 PV (mean 5.2 pV> and latenties indicating di- or trisynaptic connections. In antagonist motoneurons, the connection was mostly excitlatencies and slightly lower atory, with similar amplitudes. This work represents a rare case of “direct evidence” for both inhibitory connections between Ib afferent fibers and homonymous or synergic motoneurons and excitatory connections between these fibers and antagonist motoneurons. The term direct evidence here refers to the fact that the tendon organ afferent fibers were identified directly and not on inference drawn from electrical stimulation of the muscle nerve.

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B. Spinal Cord I. Segmental efects

Partial inhibitions of decerebrate rigidity in vastocrureus muscle observed by Sherrington (308) on mechanical stimulation applied “along the lines of attachment of the muscle” led him to assume the presence within the muscle itself of receptors responsible for this effect. The suggestion that these receptors might be tendon organs (102) came before their behavior during muscle contraction was actually verified. When Matthews (228) later described the responses of B endings, identified by him as tendon organs, to isometric or anisometric twitches and tetani, he immediately anticipated that these receptors might exert some feedback inhibitory control on muscle contraction. With Lloyd’s classic method, the actions of an afferent system on spinal motoneurons can be assessed by observing whether and how its activation, appropriately timed with respect to a stimulus eliciting a test monosynaptic reflex, affects the size of this reflex recorded from severed ventral roots. Using this method, Granit and collaborators (113, 116; see also Ref. 237; complete references in Ref. 114) demonstrated the autogenetic inhibition induced in cat ankle extensor motoneurons during contraction of their own muscle. Tendon organs were considered the most likely candidates for the role of the receptors producing autogenetic inhibition. In the initial report, Granit and Sursoet (116) mentioned that a quick stretch of the muscle, instead of a contraction, could also elicit autogenetic inhibition. However, it was soon pointed out (113, 125) that stretch alone, even under high initial tension, evoked facilitation rather than inhibition. Again with the method of monosynaptic reflex testing but with conditioning synchronous volleys elicited by precisely graded electrical stimulations of various muscle nerves, Laporte and Lloyd (201) showed that some group I afferent fibers exerted disynaptic inhibitory actions on the motoneurons of homonymous and synergic muscles. This inhibitory action of fibers within the “group I band” was widespread, being exerted not only on motoneurons receiving monosynaptic excitation from the afferents of the stimulated muscle nerve but also on distant synergic motoneurons lacking such connections. An opposite facilitatory effect was observed in antagonist motoneurons. All these actions were ascribed to tendon organs, mainly because Hunt (162) had simultaneously found that during a muscle contraction the homonymous and synergist motoneurons were inhibited, whereas those of antagonist muscles were facilitated. Tendon organs, known to be active during contraction while spindles are silenced, were thought responsible for the effects observed by Hunt, which, in addition, had a distribution very similar to that of the group I inhibitory and excitatory effects described by Laporte and Lloyd. This strongly suggested that the same afferent fibers elicited both sets of effects.


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ganized following a pattern termed “inverse myotatic Intracellular microelectrode recordings in motoneureflex,” i.e., exactly reciprocal to the pattern of Ia efrons (78,79) disclosed the cellular mechanisms of autogenetic inhibition. Afferent volleys elicited by graded fects, was not supported by the distribution of inhibition and excitation from Ib afferents to various motoelectrical stimulation of knee or ankle extensor muscle postsynaptic potentials neuron populations. This latter discrepancy has been nerves evoked inhibitory (IPSPs) in extensor motoneurons when the stimulus abundantly commented on, and there is not much more strength was increased beyond 1.2-1.3 times group I to say about it, except that the controversy should not threshold but kept below group II threshold. As these overshadow the facts. The facts remain that the main observations made by Laporte and Lloyd have been verIPSPs were superimposed on monosynaptic excitation caused by Ia afferents, they were more easily detected ified and are still providing the framework in which after reversion by a hyperpolarizing current applied to tendon organ function is investigated (e.g., see Ref. 127). the motoneuron membrane. Inhibitory potentials of Ib The widespread distribution of Ib effects has now been origin in homonymous or synergic motoneurons were recognized as the basis of an organization in which Ib either di- or trisynaptic. In antagonist motoneurons, Ib inputs are forwarded along “alternative pathways” (see afferents evoked di- or trisynaptic excitation. The fresect. VIIBZ) selected by the same supraspinal structures quency of occurrence of the homonymous inhibition was that issue the motor command. not similar in all the extensor motor pools: only 5 of 14 Intracellular recordings from lumbar motoneurons (35%) quadriceps motoneurons and 26 of 63 (41%) triwere also employed to examine the effects of natural ceps surae motoneurons had homonymous Ib IPSPs ver- activation of tendon organs by muscle contractions (115, sus 10 of 10 plantaris and 15 of 18 (83%) flexor digi117). The hindlimb was extensively denervated, with the torum longus (FDL) motoneurons. The excitatory action exception of a single muscle; ventral roots containing of antagonist Ib afferents was even less frequent, occuraxons for this muscle were cut, and contractions were ring in 3 of 21(14%) quadriceps motoneurons on stimuelicited by stimulating their peripheral end. Contraclation of biceps-semitendinosus (BST) nerves and in 1 of tions of the homonymous muscle regularly evoked auto56 (~2%) triceps surae motoneurons on stimulation of genetic inhibition in both extensor and flexor muscles, pretibial flexor nerves. In flexor muscle motoneurons and this effect was ascribed to the action of tendon orthe frequency of homonymous Ib inhibitory effects was gan afferents. The flexor sample examined by Green lower than in extensors: IPSPs were observed in only 4 and Kellerth (117) included 37 motoneurons innervating of 52 (8%) BST motoneurons and in only 2 of 36 (6%) the common peroneal muscle group (pretibial flexors) pretibial flexor motoneurons. By comparison, excitation and 7 innervating hamstring flexors. Contractions were from antagonist Ib afferents was more frequent in elicited in tibialis anterior and extensor digitorum lonflexor than in extensor motoneurons: 18 of 120 BST gus muscles. Even after suppression of any load imposed (15% ) motoneurons were excited on stimulation of quadon the muscle, i.e., without initial muscle tension, inhibiriceps nerve as were 7 of 39 (18%) motoneurons of pretitory potentials regularly appeared during contractions bial flexors on stimulation of triceps surae nerves. in 40 of the 44 motoneurons. Evidence in support of the Whether excitatory or inhibitory, the Ib afferent effects assumption that tendon organs were responsible for the were widespread, and some of the observed connections observed inhibition was not direct but rested on two sets of data, namely, 1) the contraction of a muscle is known did not conform to the expected pattern, e.g., BST afferents had an excitatory action on 6 of 31 (20%) pretibial to elicit activation of this muscle’s tendon organs (228), flexor motoneurons, whereas a motoneuron of the flexor and Green and Kellerth did verify that in their experimental conditions discharges of tendon organs occurred peroneus tertius-brevis group received inhibition from FDL. Motoneurons of the slow soleus had larger IPSPs during contractions, even when the muscle was slack; than motoneurons of fast muscles; this was the first and 2) impulses in Ib afferents are known to elicit inhibiallusion to differences in sizes of synaptic potentials re- tion of homonymous and synergic motoneurons (201). It lated to motoneuron type (see Refs. 49, 263). is therefore very likely that the autogenetic inhibition By their own account, Eccles et al. (79) confirmed of homonymous motoneurons elicited by a muscle twitch or a brief tetanus is due, at least partly, to tendon the main findings of Laporte and Lloyd (201), although they pointed out some discrepancies. Much has been organ activation within that muscle. If this interpretamade of these discrepancies, which may by now be de- tion is accepted for extensor muscles, there is no reason flated to three main points. 1) Eccles et al., using a low- that it should not be accepted also for flexor muscles. In spinal Nembutal-anesthetized preparation, saw less ef- this respect, it remains to find an explanation for the fects from flexor Ib afferents than Laporte and Lloyd in negative results of experiments with synchronous electrical stimulation of afferents in the muscle nerve. Anhigh-spinal unanesthetized preparations. Autogenetic inhibition from flexor muscles was later confirmed by other question is whether other muscle receptors may Green and Kellerth (117) working with “natural stimualso contribute to autogenetic inhibitory effects. The lation” on both low-spinal and intact Nembutal-anesthecontraction-induced activation of these receptors is tized preparations. 2) The Ib effects were exerted known, and evidence has been provided that actions of through not only di- but also trisynaptic pathways. 3) group II afferent fibers participate in autogenetic inhibiLaporte and Lloyd’s suggestion that Ib effects were or- tion (27).


650

LfiNA

2. Convergence in Ib pathways to motoneurons

Mentions of considerable variation among effects observed in different animals are found in reports on spinal actions of Ib afferent fibers (e.g., see Refs. 79 and 216). This is suggestive of a control exerted on Ib pathways either by descending tracts or/and by other afferent systems. A huge amount of work, mainly due to Lundberg and collaborators, has been performed to analyze the facilitory and inhibitory influences controlling all the known pathways of afferent information. A brief summary of this work, focusing on data related to Ib aff erents, is attempted here. The main methods used in these investigations include monosynaptic reflex testing (see sect. VIIA) and the spatial facilitation technique (see Ref. 213) applied to demonstrate the convergence of two effects on a target, here a set of interneurons interposed in Ib pathways. The aim is to detect whether two afferent systems, a and b, evoking similar effects in a given motoneuron use separate or common pathways. Each system on its own elicits discharges from a number of interneurons plus a subliminal activation in others. If there are two separate sets of interneurons, then the postsynaptic potential (PSP) recorded in the motoneuron on simultaneous activation of a and b cannot be larger than the algebraic sum of the PSPs elicited by each system on its own. A larger PSP indicates the discharge of additional interneurons, common to both pathways, and led to discharge by addition of subliminal effects when a and b are stimulated together. This interpretation rests on the assumption that all PSPs recorded in motoneurons sum linearly. In preparations under light Nembutal anesthesia, stimulation of the cerebral cortex in the postsigmoid gyrus was found to increase the inhibitory action of FDL muscle afferents on the triceps surae monosynaptic reflex. In triceps surae motoneurons, Ib IPSPs elicited by FDL or plantaris nerve stimulation showed a marked increase on combined stimulation of the motor cortex. Enhancement by cortical stimulation of Ib excitation from extensor to flexor motoneurons was occasionally observed. None of the effects of cortical stimulation on Ib actions was present in preparations with transected pyramidal tract (220). Actual convergence on interneurons of corticospinal and muscle afferents was observed by Lundberg et al. (218). Similar corticospinal influences on Ib actions were later observed in reflex pathways of the cat forelimb, with short delays suggesting a monosynaptic connection between corticospinal fibers and interneurons relaying Ib input (169). Actions parallel to those of the corticospinal tract were exerted by the rubrospinal pathway in preparations under chloralose plus light Nembutal anesthesia. All the effects of Ib afferents, whether excitatory or inhibitory, were enhanced on combined stimulations of muscle nerves and of the red nucleus (142). Moreover, rubrospinal facilitation allowed expression of Ib effects that were hardly visible when tested in isolation. This work represents an important step in our understand-

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ing of the organization of spinal Ib pathways because it led to the idea that descending motor commands can open “alternative pathways” for Ib inhibitory or excitatory effects, depending on the pattern of the commanded movement. The time course of the facilitation suggested a monosynaptic projection of rubrospinal fibers on Ib interneurons, and monosynaptic rubral excitation was actually observed in some of them (144). In cervical segments, a direct excitatory connection of the rubrospinal tract with interneurons mediating group I effects from forelimb muscles was also demonstrated (169). In contrast, Ib pathways are tonically depressed in decerebrate preparations (82) mainly by the influence of the dorsal reticulospinal system (94) and of the noradrenergic reticulospinal system (8). Some propriospinal neurons in the cervical segments of the spinal cord have long axons coursing toward lumbar segments in the dorsal half of the lateral funicle. The effects of these neurons on Ib pathways were tested on preparations in which all the supraspinal fibers other than the long propriospinal fibers had been eliminated. Stimulation of these fibers was then found to facilitate about two-thirds of the disynaptic inhibitory or excitatory Ib PSPs recorded in lumbar motoneurons. Monosynaptic coupling of propriospinal fibers with interneurons of the Ib pathway was demonstrated (182). At segmental levels, other afferent systems influence transmission in Ib pathways. This was demonstrated in low spinal preparations under chloralose and light Nembutal anesthesia (215,216). Conditioning volleys in low-threshold cutaneous afferents facilitated the di- and trisynaptic Ib inhibitory pathways to homonymous and heteronymous motoneurons (see also Ref. 264). Excitatory PSPs (EPSPs) evoked in flexor motoneurons by Ib afferents from extensor muscles were also facilitated by impulses in cutaneous fibers. The time course of the effect suggested a disynaptic linkage between cutaneous afferents and Ib interneurons. Facilitation of Ib effects by low-threshold cutaneous afferents appeared more efficient in forelimb reflex networks than in their hindlimb counterpart (169). The functional significance of convergence between cutaneous and Ib input might be very important in the control of exploratory movements by hand or foot (216). It is not known yet which cutaneous territories are innervated by the fibers contributing facilitation to Ib pathways (but see sect. VIIB6). Afferents from the posterior knee joint nerve represent another source of facilitation of Ib pathways from hindlimb muscles to motoneurons. The patterns resemble those of cutaneous facilitation (215, 217), but here the interpretation of the effects was not so easy. Fibers in the posterior knee joint nerve do not come exclusively from joint receptors, some are from tendon organs and spindles of the popliteus muscle (119, 206, 242). However, on consideration of electrical thresholds for recruitment of the fibers producing the facilitation of Ib effects, Lundberg et al. concluded that a substantial


July m%?

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TENDON

portion of this facilitation was due to joint afferents connected with Ib interneurons through a disynaptic linkage. The two sets of data (215-217) suggest that information from joint and skin afferents may participate in segmental regulations through either Ib or/and flexor afferent reflex systems. Selective activation of Ib fibers by the method of Jack (173) was used in decerebrate preparations to show that Ib afferents from contralateral muscles participate in the crossed extensor reflex (22). In low-spinal preparations under chloralose anesthesia, contralateral group I afferents from either quadriceps, hamstring, or triceps surae facilitated the excitatory effects of Ib afferents from either the homologous flexor muscles to extensor motoneurons or from extensor muscles to flexor motoneurons in about one-half of the tested combinations. The facilitation was not very efficient, requiring repetitive stimulation of the contralateral nerve. Very few facilitatory actions of Ib inhibitory effects were observed (133). From this catalogue of convergent influences on Ib spinal pathways, two notions emerge. First, no evidence has been found so far of any “private” pathway specifically subserving the distribution of information from hindlimb tendon organs to lumbosacral motoneurons. On the contrary, this information is coprocessed with information from skin and joints. The functional significance of this convergence is that distribution of Ib inhibition to motoneurons may be “helped” by a variety of other inputs. Second, the gating of Ib pathways by cortico-, rubro-, and reticulospinal tracts, i.e., from key centers of motor control, suggests that reflex Ib actions are seldom allowed independent expression but rather are channeled into “alternative pathways” as required by each precise motor command. An even tighter gating is achieved by the remarkable prevalence of presynaptic inhibition of Ib fiber terminals within the spinal cord (see

sect.

v11B4).

Muscle afferents from forelimb muscles cannot be distinguished on the basis of electrical stimulation threshold (287), and for this reason the studies on projections of forelimb afferents in the cervical spinal cord concern group I afferents as a whole (see Ref. 15). A generally accepted implicit assumption is that disynaptic IPSPs elicited in cervical motoneurons by stimulation of forelimb muscle nerves at group I strength are due to Ib afferent effects. Data on this pathway came from studies on the effects of corticospinal volleys on reflexes from muscle afferents (169). Propriospinal interneurons were subsequently identified that are located in the third and fourth cervical segments (C,-C,) of the spinal cord and project on forelimb motoneurons. These premotor neurons, integrating a variety of central and peripheral inputs, act as major elements of control in forelimb voluntary movements (see Ref. 4). The C&-C4 interneurons are inhibited by group I afferents from forelimb muscles (6) via a disynaptic pathway involving neurons located in the medial part of the base of dorsal horn (7). Selective activation of either Ia or Ib afferents from five forepaw extensor muscles evoked fo-

ORGANS

651

cal synaptic potentials in this region (111; see also Ref. 5). This is the only published instance of selectively activated tendon organ afferents in the cat forelimb. 3. Identi&ed interneurons in Ib lumbar circuits

Most of our knowledge on these interneurons was provided by the investigations of Jankowska and collaborators. In elaborate experiments, they used a variety of techniques to ascertain the origin of afferent input to the studied interneurons, their location, and their projections to further targets. This work led to the identification of the “nonreciprocal” inhibition mediated by Ib interneurons. The first reason for adopting this terminology was the discovery that Ia afferents from spindle primary endings in triceps surae and plantaris muscles exert autogenetic inhibitory effects on homonymous and synergistic motoneurons, in addition to their well-known excitatory actions (97). Careful verifications that this inhibition could be ascribed to Ia afferents involved selective nearly synchronous activation of spindle primary endings by brief stretches of -30 pm amplitude that did not act on tendon organs. Such stretches elicited di- and trisynaptic IPSPs in 80% of the examined motoneurons. Hyperpolarization of motoneuron membrane was often necessary to clearly see the IPSPs because they were superimposed on monosynaptic EPSPs. Inhibitory effects from Ib afferents, observed on selective activation of tendon organs, were much stronger than Ia inhibition, which suggested that inhibition from spindles operates primarily to support inhibition from tendon organs (97). The second step was the demonstration that Ib and Ia inhibitory inputs from knee flexor and extensor muscles and from ankle extensors converge on the same interneurons. These interneurons were labeled by intracellular horseradish peroxidase and reconstructed to demonstrate their location in laminae V-VI of the intermediate zone of the lumbar spinal cord and their projection to motor nuclei (70, 181). Some of these interneurons were coexcited by Ia and Ib inputs, whereas others were coinhibited, and a third subgroup was excited by the one and inhibited by the other input. Moreover, the distribution of Ia inhibition in motoneurons of triceps surae and plantaris muscles was parallel to the distribution of Ib inhibition. The term nonreciprocal inhibition was then introduced because it became necessary to distinguish the Ia-Ib autogenetic disynaptic inhibition from the reciprocal disynaptic inhibition of motoneurons by Ia afferents from antagonist muscles (184). With the spatial facilitation technique, subsequent studies demonstrated that Ia and Ib afferents from several muscles exerted inhibitory actions on motoneurons through the same interneuron (130,183). This has been termed “shared reflex pathways” and led to the conclusion that “the information forwarded to individual motoneurones is therefore the ensemble picture of the length and tension of many muscles” (130). It is unlikely


652

LfiNA Joint

I nterosseous

f,r.aa

co. gr Group

I

Group

I

Y 0 Motoneurone

FIG. 7. Summarizing diagram of sources of input to population of interneurons mediating nonreciprocal inhibition of motoneurons. Open and solid arrowheads (superimposed) represent excitatory and inhibitory inputs, respectively. Diagram is based on data from following references: 1) 37,79; 2) 37,130,183; 3) group I input from contralatera1 limb (Co), 133; 4) 128; 5) 215,216; 6) 215,217; 7) 131; 8) flexor reflex afferents (fra), 128; 9) 182; 10) 169,220; 11) 142; 12) 94; 13) noradrenergic (na) reticulospinal system, 8. [From Harrison and Jankowska

WOI that any particular variable is encoded in this information whose practical significance for individual motoneurons might simply be that any contraction and/or any movement, whether active or passive, may evoke widespread inhibition. The function of this general inhibition is not yet elucidated, but we have seen that it is channeled by supraspinal influences (see sect. VIIBZ), and, in addition, it is controlled by mutual inhibitory interactions between nonreciprocal interneurons (37) that might act to restrict the target field of Ib inhibition (see a possible example in humans in sect. VIIB~). The same information is forwarded to Clarke’s column where it evokes inhibition in DSCT cells (145,146). Disynaptic IPSPs elicited by group I afferents from various muscles were recorded in DSCT cells after lesions of the dorsal funiculi interrupted the transmission from primary afferent fibers to those interneurons located at the same level as Clarke’s column. Interneurons mediating the nonreciprocal inhibition of motoneurons were shown to send collateral branches in the lateral funiculus, projecting on DSCT cells. These cells therefore, like motoneurons, receive both monosynaptic excitatory and disynaptic inhibitory input from group I muscle afferents (see sect. VW). In summary, Figure 7 shows the diagram drawn by Harrison and Jankowska (128) after a systematical investigation of all the possible sources of input to nonreciprocal inhibitory interneurons. In their study, Harrison and Jankowska carefully verified the actual action of all these inputs on their interneurons. They found

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convergence from all th e inputs that have been mentioned in section v11B2 plus a few others, mostly by monosynaptic or mono- and disynaptic linkage. The main conclusion of this investigation is that interneurons mediating nonreciprocal inhibition of motoneurons now appear as sites of complex integration of central and peripheral information. All the inputs indicated in Figure 7 did not converge on every interneuron, but no precise pattern of convergence emerged from a probability analysis carried out on data from 18 interneurons (129). The authors concluded that possibly the organization of the system depended on random connections of a given input with random samples of the interneuronal population. It is not certain whether this disappointing conclusion, based on the analysis of a relatively small sample, can be generalized. The organization patterns that might emerge from random connections are not obvious. Possibly the selection among the multiple possibilities and combinations of inputs transmitted by nonreciprocal interneurons depends on specific patterns of motor commands gating the information through alternative pathways. Further studies are needed to understand how the information from mu scle afferents is processed in the spinal cord, but the available data do not point to simple length and/or force feedback systems. Another question is how information from tendon organs is processed in circuits other than the nonreciprocal inhibitory system. The observed heterogeneity in the distribution of nonreciprocal inhibition to motoneurons of the soleus pool (186)may not be due solely to random factors. Harrison and Jankowska (128) were aware of the fact that the criteria used for identifying their interneurons left out a number of laminae V-VI interneurons receiving group I input. Nothing is known of the interneurons wi thout Ia-Ib convergence, except the fact that they exist, and, for in stance, in the sampl .e examined by Jankowska et al. (181), there were 36% of interneurons with selective excitatory and/or inhibitory input from Ib afferents of triceps surae and plantaris. In addition to nonreciprocal inhibitory interneurons, there are at least three other categories of interneurons receiving Ib inputs: I) first-order interneurons in the trisynaptic inhibitory pathway to homonymous motoneurons, 2) interneurons mediating the excitatory effects from Ib afferents on motoneurons, and 3) interneurons mediating the presynaptic inhibition “given” by Ib afferent fibers (see sect. v11B4). Further work is needed to discover the properties of these interneurons and to understand how they cooperate with the nonreciprocal inhibition system. 4. Pres ynaptic inhibition

Presynaptic inhibition of transmission mary afferents in the spinal cord is thought by depolarization of the terminal portions [primary afferent depolarization (PAD)], reduce the release of transmitter. The PAD

from prito be caused of the fibers which could is probably


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produced through axoaxonic synapses connecting interneuron terminals with primary afferent terminals (63). A comprehensive account of the methods used in the study of presynaptic inhibition and of their main results can be found in the review by Schmidt (303; see also Refs. 15,289), which in addition gives a straightforward view of the many unsolved questions. Presynaptic inhibition in the Ib system was described by Eccles et al. (81) as a “general negative feedback of Ib afferent fibres onto themselves.” This definition referred to the fact that the Ib afferent fibers of all the tested muscle nerves are sources of presynaptic inhibition for virtually all the ipsilateral Ib fibers, a phenomenon that is not yet clearly understood. Other segmental sources of PAD for hindlimb Ib fibers include group II and III muscle fibers and cutaneous afferents from both ipsi- and contralateral hindlimbs. The PAD in Ib fibers is also elicited by stimulation of the sensorimotor cortex, of two different regions in the brain stem, of the VIIIth cranial nerve, and of the vestibular and fastigial nuclei; in decerebrate preparations, stimulation of the anterior cerebellar cortex is also effective (see complete references in Ref. 303). The rubrospinal tract elicits PAD in Ib and cutaneous afferent fibers (143) in addition to its action on interneurons interposed in Ib pathways (see sect. VIIBZ). In addition to Ib fibers from ipsilateral extensor and flexor muscles (81), other target fibers in which Ib afferent fibers from flexor and extensor muscles produce PAD are Ia fibers of flexor and extensor muscles (mainly by Ib afferents from ipsilateral flexor muscles) and cutaneous fibers (see Ref. 303). It appears functionally significant that Ia fibers receive PAD from Ib fibers while the reverse does not occur. Presynaptic inhibition might thus control the balance of Ia and Ib inputs in the circuit of nonreciprocal inhibition. The shortest pathways mediating presynaptic inhibition of group I fibers are known to be trisynaptic (185; see Ref. 303), and the minimal number of distinct interneuronal populations mediating PAD of group I fibers could be two to six (38). Convergence of cutaneous and Ib afferents on interneurons mediating PAD of Ib afferents has been demonstrated, indicating that these two sources of PAD share the same pathway (see Ref. 188). In contrast, there is evidence suggesting that different pathways mediate the PAD of Ia and Ib fibers from extensor muscles (38, 291). Current investigations concentrate on attempts to identify the interneurons mediating the presynaptic inhibition of Ib fibers (292). Some of these interneurons might represent intersections between pathways of pre- and postsynaptic Ib inhibition (211,312). This is probably not the case for the interneuron of the disynaptic nonreciprocal pathway (38), but there is a possibility that the firstorder interneuron of the trisynaptic pathway participates in PAD pathways (see Refs. 185,290, 291, 293). Efferent activity in muscle nerves organized in a pattern resembling the pattern of locomotion can be obtained in decorticated preparations immobilized by curare (259). Observations of cyclic changes in the excitabil-

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ity of Ia and Ib fibers, related to the fictive locomotor cycle, suggest that the central pattern generator for locomotion can modulate presynaptic input to group I fibers during fictive locomotion (75; see also Ref. 74). Natural activation of tendon organ afferents by muscle contraction has been long known to elicit presynaptic inhibition of group I fibers (72). More recently, an appreciable reduction of autogenetic inhibition was observed in motoneurons of triceps surae during prolonged contractions of the medial gastrocnemius muscle; however, on abrupt increase of contractile force, inhibition was restored to decline again, even though contraction was maintained at this higher level. Inhibitory information forwarded to motoneurons thus signaled essentially the onset of contraction and subsequent rises in contractile force (346). During similar contractions, PADS were recorded in homonymous Ib fibers, indicating that presynaptic inhibition of Ib afferents could account for the decline of autogenetic inhibition (345). In this instance, presynaptic inhibition acted as a filter, cutting off the transmission of inhibitory informations about force development on prolonged contractions. 5. Rejexes

Traditional views tended to associate the discharges of tendon organs with reflex reactions described by Sherrington (308), namely, the lengthening reaction of decerebrate preparations and the claspknife reflex seen in chronic spinal preparations. The lengthening reaction appears in tonically active knee extensor muscles on attempt by the experimenter to flex the knee, i.e., to lengthen the contracting muscles. At some point, the resistance yields, i.e., a partial inhibition of contraction allows the muscle to lengthen and to remain at the new length when released. The lengthening reaction was long thought to occur when the muscle tension had reached the supposedly high threshold of tendon organs, whose discharges then caused inhibition of contraction. The same mechanism was thought to account for the “clasp-knife reflex,” a sudden suppression of resistance to forced knee flexion, which is occasionally also observed in decerebrate preparations (25). In fact tendon organs have a very low threshold for contractile force (see sect. v), and they may be expected to discharge in the contracting muscles even in the absence of lengthening effort applied by the experimenter. The mechanisms underlying the lengthening reaction and the clasp-knife reflex are not fully understood, but they are unlikely to represent “pure” Ib reflexes (see discussion in Ref. 229). Alternative explanations have been proposed, involving spindle secondary afferents (47,48) or muscle free endings (see discussion in Ref. 59; see also Ref. 299). The lengthening reaction is associated with a reflex extension of knee and ankle extensor muscles in the opposite limb, called Philippson’s reflex by Sherrington (308) and known as the crossed extensor reflex. There is


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presently no certainty about the receptor responsible for this reflex (21,22,33,139,257,258). Possibly concurrent discharges from several types of muscle receptors, including tendon organs (ZZ), are necessary for eliciting this reflex. One reflex effect for which discharges from tendon organs might provide the relevant input is the feedback control of muscle contraction. Under the assumption that the regulated variable could be the force output, ideas inspired by the control system theory suggest that an automatic negative force feedback would be useful in the control of muscle contraction (157,158). This kind of system implies an automatic control device (i.e., inhibition of motoneurons) that is turned on by an “error signal” (i.e., tendon organ discharge). A first difficulty in viewing the Ib reflex circuit as a servomechanism is that the control device is not automatic, being gated by descending pathways that converge on the interposed interneuron and by presynaptic inhibition (the spindle servo is a better approximation of an automatic control because the monosynaptic connection of Ia fibers with motoneurons is relatively less dependent of descending influences). The effect of gating is to modulate the sensitivity (gain) of the system, which is not convenient if muscle force has to be kept constant but may become an advantage when force output is continuously varying, as occurs under natural conditions (an example of gain varying with the force of voluntary contraction has been observed in humans; see sect. VII&Q. The same problems would be met in a system in which the controlled variable would be muscle stiffness instead of muscle force (155). The second difficulty concerns the mediation of the “error signal” through an interneuron that is a site of multiple convergence, mixing together inputs from tendon organs of several muscles, muscle spindles, skin, and joints. The actual content of the error signal forwarded to motoneurons will depend on the balance between the different inputs, which in turn depends on their modulation by presynaptic inhibition. Experimental demonstration of a reflex feedback controlling the force of muscle contraction was provided by Houk et al. (160) in a decerebrate preparation. A small portion of the motor axon supply to the soleus muscle was stimulated in a cut ventral root filament, either alone or superimposed on a stretch reflex contraction. The measured increase in muscle force was smaller in the latter case, because the Ib input elicited by the superimposed contraction partially inhibited the stretch reflex. The resultant force was therefore smaller than the sum of the forces developed separately by the stretch reflex and by the stimulation of the ventral root filament. However, the gain of this feedback loop was rather low, possibly because Ib pathways are depressed in decerebrate preparations (82, 94, 140; see also Ref. 298). A recent study confirmed the lowness of gain in the decerebrate, but significantly higher gains were found after transection of the spinal cord and also in decerebrate preparations with chronic contralateral cerebral lesions (168, 174). In humans, the presence of a “force regulator of modest gain” was assumed to partially

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compensate for the effects of muscle fatigue (193). On the basis of a mathematical speculation it was recently suggested that a given interneuron mediating nonreciprocal inhibition projects to ~5% of motoneurons in a given pool (132). The convergence of cutaneous inputs in Ib spinal pathways (see sect. VIIBZ) suggests that they might participate in reflex force regulation. In this context, the study of Johansson and Westling (189) on human precision grip is interesting. When a small object is seized to be lifted between thumb and fingers, a delicate balance has to be kept between the force of the grip and the vertical lifting force (load force). Johansson and Westling recorded afferent responses from cutaneous receptors, together with load force and grip force, during tests where the object was covered with either sandpaper, suede, or silk. These substances have different structures, eliciting different patterns of cutaneous afferent discharges. Correlations between changes in cutaneous afferent discharges and variations of grip and load forces were observed, suggesting that tactile input was used to trigger reflex adjustments of the grip-toload force ratio. In conclusion, the available evidence supports the assumption of a reflex feedback control of contraction most probably mediated by tendon organ discharges, with the possible cooperation of other inputs. Force is easily measurable, but it is not certain whether it is the actually regulated variable, because many other inputs converge in the Ib pathways. There is an obvious need for a new model different from the servo models that do not accomodate all the known features of Ib circuits. Possibly a better fit with recent data could be obtained in models including parallel networks that would take into account the gating and channeling of Ib input through alternative pathways, depending on the motor task, and the input from other receptors that may contribute to force detection and regulation. It should also be kept in mind that, in addition to the Ib system, other negative feedback circuits, also gated by supraspinal influences, may be triggered by the discharge of cr-motoneurons: I) recurrent inhibition, 2) disfacilitation due to slowing or pause in spindle primary ending discharges (in the absence of fusimotor drive), and 3) reciprocal inhibition due to spindles of stretched antagonist muscles during a shortening contraction. None of these events is contraction specific, but they might nevertheless contribute to regulation of contraction. 6. Studies in humans Experiments with humans allow unique opportunities for investigation of interactions between spinal pathways and voluntary contractions. The method used, derived from the monosynaptic reflex testing, is based on systematical observations of the effects of conditioning stimulations on the H-reflex. There are no data on the proportion of group Ia and Ib fibers in human muscle nerves, on their excitability, or on their conduction


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velocity. It is generally assumed that, in lower limb muscle nerves, Ib fibers have slightly higher thresholds for electrical stimulation than Ia fibers. On this assumption, the organization of Ib spinal circuits in humans first appeared similar to that observed in cats, including inhibition of homonymous and synergic motoneurons by Ib fibers from knee and ankle extensor muscles (24,261, 262) and facilitation of extensor motoneurons by Ib fibers from ankle flexor muscles (261). The effects of cutaneous afferents on human Ib reflexes provide good examples of the possibilities offered by convergence in Ib pathways. At rest, a cutaneous stimulation of the ipsilateral foot sole selectively depresses the inhibitory effects of Ib fibers from triceps surae on quadriceps motoneurons, whereas the depression of triceps surae motoneurons is not affected (261). In contrast, stimulation of the contralateral foot sole facilitates the transmission of Ib effects to quadriceps motoneurons (23). The functional significance of these effects is most likely related to locomotion: during the stance, it seems useful to limit the inhibition of quadriceps as long as the foot sole is in contact with the ground. During voluntary contractions, the Ib inhibition of homonymous motoneurons is depressed, probably by actions from supraspinal centers, since the depression is already present before the onset of contraction (98). The depression increases with the strength of the contraction, which means that the gain of the Ib force feedback varies during voluntary contraction. Cutaneous stimulation, applied in a restricted zone of the anterior portion of the foot sole, can nevertheless facilitate homonymous Ib inhibition in triceps surae motoneurons during a voluntary contraction of this muscle. This facilitation might be used to stop an exploratory movement of the foot when an obstacle is met (260). Similar facilitation of Ib effects by cutaneous afferents was found in the upper limb on motoneurons of muscles controlling hand movements (57). Finally, a facilitation of Ib inhibition in synergic motoneurons, concurrent with the depression of homonymous inhibition, has been observed during a selective contraction of triceps surae. This example is particularly demonstrative of the choices that can be operated among the targets of the widespread Ib inhibition by different patterns of motor command (98). 7. Effects on y-motoneurons

The demonstration that Ia and Ib inputs converge on the same interneurons (see sect. VIIB~) prompted hypotheses about a fusimotor control indirectly exerted on tendon organ actions (183,214). It is therefore of interest to consider the autogenetic effects of muscle contraction on y-motoneurons (90-92). Discharges in triceps surae y-axons were recorded from nerve filaments during partial isometric contractions of the homonymous muscle in decerebrate preparations (92). A twitch or a brief tetanus produced an inhibition of the sustained discharge in 22 of 47 examined y-axons. Not all the

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y-motoneurons were inhibited (or disfacilitated) by contraction, some were unaffected (34%), and others showed a period of facilitation either isolated or following the inhibition. Similar experiments, comparing the effects of FDL and gastrocnemius-soleus contractions, showed that less inhibition was induced from synergic than from homonymous muscles (90). In such experiments it was of course impossible to distinguish static from dynamic fusimotor discharges. Suggestive, albeit indirect, evidence pointed to tendon organs as the receptors responsible for the inhibition of y-discharges. However, this assumption stands in contradiction with the negative observations of Appelberg et al. (12), who reported that electrical stimulation of group I afferents was virtually without effect on y-motoneurons. Further explorations of the interactions between Ib afferent input and fusimotor control are required to fully understand the consequences of the convergence of Ia and Ib afferents in nonreciprocal inhibition pathway. C. Cerebellum

Patterns of cerebellar neuron discharges suggest that information about muscle contraction is a major component of the proprioceptive input to cerebellum (e.g., see Refs. 95, 134, 170, 171,301,302,311,329). Cerebellar cortex receives input from muscle receptors through spinoolivocerebellar pathways terminating as climbing fibers and spinocerebellar pathways terminating as mossy fibers (see Ref. 87). Specific connections with tendon organ afferents from hindlimb muscles have been recognized in cells of origin of the latter pathways. These include two uncrossed pathways, the DSCT and cuneocerebellar tract, carrying information from the hindlimb and forelimb, respectively, and two crossed pathways, the ventral spinocerebellar tract (VSCT) and rostra1 spinocerebellar tract. The review by Oscarsson (253) gives a classic account of the functional organization of those spinocerebellar paths involved in transmission of information from tendon organs (see also Refs. 31,238,272), and only the main data are summarized here. Among other spinocerebellar paths, only the uncrossed tract described by Aoyama et al. (11) is known, so far, to carry information from group I muscle afferents. Clarke’s column, in the medial portion of lamina VI between spinal segments T, and L,, has long been known to contain the cells of origin of the DSCT, some of which receive monosynaptic excitation from Ib afferent fibers from a single muscle or muscle group (223,239). Other, more numerous, DSCT cells are monosynaptically excited by Ia fibers and spindle group II fibers (80, 202, 203, 239), whereas joint and cutaneous afferent fibers are distributed to still other subgroups of DSCT cells (see Ref. 206; see complete references in Ref. 253). An important point is that distinct subgroups of DSCT cells are relaying the inputs from spindles and from tendon organs (219; see Refs. 238, 252). Both connections are remarkable by their efficacy, probably due to the giant


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boutons of the synapses between group I fibers and DSCT cells (327, 330). In addition to the monosynaptic excitation, DSCT neurons also receive disynaptic inhibition from group I (Ia and Ib) muscle afferents (see references in Ref. 253; see also Ref. 250). Interneurons mediating this inhibitory action were recently identified in laminae V-VI of segments L,-S, and found to coincide with interneurons of the nonreciprocal inhibition (145,146; see sect. ~11233). Consequently, the multiple inputs converging on nonreciprocal interneurons must be counted among sources of inhibitory influences on DSCT cells (128). The DSCT fibers reach their targets in the cerebellar cortex of the anterior lobe and paramedian lobule via the inferior peduncle. On their way they give off collaterals to nucleus Z, which is the relay of tendon organ input to cerebral cortex (241; see sect. VIID). Cells of origin of the cuneocerebellar tract also receive input from group I muscle afferents, but since there are so far no reliable criteria for distinguishing Ia from Ib components in afferent volleys from forelimb muscle nerves, nothing is known of the connections of specific Ib input with these neurons. The cells of origin of the VSCT include not only the “border cells” of the external margin of the ventral horn (52,65) but also cells located in the lateral parts of laminae V, VI, and VII (see Fig. 1.3 in Ref. 39). The axons of VSCT neurons immediately cross the midline to ascend the contralateral lateral and ventral column. They enter the cerebellum via the superior peduncle and cross the midline again to end in the cortex of the anterior lobe. The decussation does not involve the total population of VSCT fibers, with some fibers ending on the side opposite to the cells of origin. Early studies suggested that Ib input was the major component of muscle afferent input to VSCT cells, many of which receive converging monosynaptic excitation from Ib fibers of several muscles. It is now recognized that, in addition, Ia and high-threshold muscle afferents also contribute input to VSCT cells (80, 221, 251). The converging connections may be excitatory from Ib and inhibitory from Ia, excitatory from both systems, or inhibitory by group I of Ib excitation (205). In addition, the VSCT cells are controlled by corticospinal, rubrospinal, reticulospinal, and vestibulospinal tracts. The VSCT tract is considered to carry “information about the activity evoked in segmental reflex arcs by different descending paths. . . and by different segmental paths like the muscle spindle and tendon organ afferents and the Renshaw cells” (87). The information carried by the indirect spinoolivocerebellar tract is considered to concern mainly flexor reflex afferents and cutaneous afferents (87). There is, however, evidence suggesting that low-threshold group I afferents from hindlimb muscles may send projections to the dorsal accessory olive through the ventral spinoolivary tract (14) and that contraction-induced actions on Purkinje cells may be mediated by the climbing fiber system (171). Clinical observations have long made it clear that

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the cerebellum controls the ability to adjust and coordinate muscle contractions, and available data show that the relevant information from contraction-activated tendon organs reaches the cerebellum via several different routes. The possibility of a specific processing of information from tendon organs in cerebellar circuitry might be provided by the separation of “two channels of information (in DSCT) one for muscle spindles and one for tendon organs” (252). D. Cerebral Cortex

The access of information from tendon organs to the cortex was recently demonstrated by McIntyre et al. (240) in chloralose-anesthetized preparations. They used the method of muscle vibration (173) to selectively increase the electrical stimulation threshold of Ia fibers from muscles of the triceps surae. After a period of muscle vibration, a single stimulus applied to the muscle nerve (with a strength not exceeding 1.5 times the group I threshold) evoked a small-amplitude potential from the post-sigmoid gyrus of the contralateral pericruciate cortex. In addition, discharges from cortical neurons could be recorded by extracellular microelectrodes below the surface of the evoked potential focus. This site corresponds to the region where Landgren and Silfvenius (197) had found projections of group I impulses from the cat hindlimb. In a further study, McIntyre et al. (241) showed that the pathway of Ib input from the spinal cord to the motor cortex includes DSCT neurons sending a collateral to nucleus Z. Afferents from distal muscles contributed a large fraction of the Ib input to nucleus Z (see Ref. 198). Discharges of nucleus Z neurons, showing a tendon organ-like pattern, were evoked by m uscle con traction. These neurons could be activated antidromically from the contralateral thalamus, but they were different from the cells responding to stimulation of Ia fibers (see Ref. 224). The absence of convergence of Ia and Ib inputs on nucleus Z neurons suggests that information on muscle length and contraction remains separate at least as far as the thalamic relay. Observations on the projections of forelimb Ib afferents are so far lacking. In the cuneate nuclei, which relay group I information from forelimbs, very few (5%) cells were found to display a tendon organ-like pattern of discharge, and it remains uncertain whether they project to the thalamus (287). Further work is required to identify the relays allowing access of forelimb tendon organ discharges to the cerebral cortex. E. Perception

The demonstration that messages from tendon organs reach the highest levels in the nervous system hierarchy points to their participation in conscious sensations. What kind of perception might be subserved by these contraction sensors? We are not commonlv aware


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of a muscle contraction. Sensations related to contraction are usually referred to limb segments and groups of muscles. Whether such sensations arise from the messages of specific receptors or from internally generated messages called corollary discharges has been the subject of long discussions that led to a compromise: perception of posture and movement depends on coprocessing of peripherally and centrally generated information (see reviews in Refs. 103, 191, 234, 230, 231). Appreciation of the force developed in a voluntary contraction is thus thought to rely on a peripheral “sense of tension” derived from muscle receptors combined with a “sense of effort” derived from motor commands. Attempts to assess the role of tendon organs in force perception have to put up with two handicaps. First, it is impossible to devise an experimental situation in which tendon organs would be the exclusive source of information. Skin and joints can be anesthetized, but spindles cannot be eliminated from within the contracting muscle. Experiments showing that muscle receptors allow perception of tension were performed by Roland and Ladegaard-Pedersen (285; see also Refs. 283, 284) with blindfolded subjects instructed to compress calibrated springs between index and thumb. Having first compressed a spring to a given length decided by the experimenter, the subject was then asked to reproduce the same force with a second spring of different stiffness. The force-matching performance was fairly good at different muscle lengths and remained unaffected by skin and joint anesthesia, which demonstrated that muscle receptors (i.e., not tendon organs on their own but muscle receptors including tendon organs) can provide reliable information about contractile force. The existence of a sense of tension, i.e., a contractiongauging sense, was further supported by experiments in which the subjects were able to match the force developed by a partially curarized and anesthetized hand with the other noncurarized and nonanesthetized hand, that is, under conditions of abnormal relation between command and force development. In addition, the demonstration of a sense of effort, called by the authors “memory for motor orders,” was provided by asking the subjects to match, with the noncurarized hand, the subjective effort (and not the actual force) sustained by the curarized hand. A substantial increase of the force developed by the noncurarized hand was then observed. The second problem is that the relevant information for perception concerns the force exerted on joints, i.e., the force developed at the muscle tendon, and we have seen that tendon organs are not very good at measuring this force (see sect. v). This might explain the difficulty experienced by subjects and the inaccuracy observed in weight- or tension-matching experiments (235), that is, in a situation different from those investigated by Roland and Ladegaard-Pedersen. It does not necessarily follow that tendon organs cannot participate in perception of force. It is neither known where corollary discharges are produced nor where they are decoded. On the basis of psychophysical observations (105, 106, 235, 236), Mat-

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thews (230) argued that corollary discharges were “used in preference to the apparently equally suitable signals from the tendon organs” in subjective assessment of the heaviness of a lifted object (see also Ref. 191). The first evidence proposed to support this statement was the fact that the perceived heaviness of a weight increases in parallel with muscle fatigue (192,235). It is not clear why tendon organs should be discarded in this instance, since they monitor the contraction of motor units with a particular sensitivity for changes in force output (see sect. v). The force decline caused by fatigue might well result in a reduction in Ib afferent traffic, which, even without a precise measurement of the decline, might be significant for the central nervous system because it reads “motor output declining.” Such information can be provided only by muscle receptors. Information derived from motor command may concern the number and type of recruited motor units and possibly also their frequency of activation, but how could a change in the motor output of the recruited units, whether due to fatigue or to potentiation of contraction, be reflected in corollary discharges? The messages from tendon organs of a fatiguing muscle might contribute to the sensation that an increased effort is required if the task has to be pursued, hence to the sensation of increased heaviness. The second evidence was the lessening of perceived heaviness observed when a tonic vibration reflex is induced in a weight-supporting muscle. In this case, the reflex contraction superimposed on the weight-supporting contraction will cause an increase in Ib afferent traffic (and in inhibitory influences on motoneurons), whose message might now read “motor output increasing; turn off some motor units.” Again, this kind of message would be quite appropriate for eliciting the sensation that the task requires less effort and hence a reduction in the perceived heaviness. Along the same line, one could contend that messages from tendon organs participate in the sensation of increased heaviness of an object lifted by a locally curarized muscle (106, 236). Actual perception certainly implies more elaborate processes than the simple reading of “messages” carried by tendon organ discharges. It remains that this kind of information appears adequate for eliciting variations in sensations of heaviness produced by fatigue or by perturbation of muscle contraction. Evidence has not been produced so far that such information is disregarded in the shaping of sensation (see Refs. 62,297,336). It is very likely that, as demonstrated for position sense (104, 233), associated messages from skin, joints, and muscle receptors, including tendon organs, are used for the subjective appreciation and voluntary control of contractile force. VIII.

CONCLUSIONS

Tendon organs are said to monitor muscle contraction because they are silent at rest and start discharging as soon as a motor unit starts contracting. This has been repeatedly demonstrated in vitro with isolated recep-


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tors and in vivo with anesthetized preparations, freely moving animals, and humans. Although tendon organs do not behave as simple dynamometers, they can signal quite small variations of contractile force. Are such functional properties suitable for the control of muscle contraction? They seem at any rate compatible with a simple view of autogenetic inhibition in which input from tendon organs, elicited by the contraction of the first recruited motor units, exerts inhibitory influences on homonymous motoneurons and restrains the recruitment of further units, thereby smoothing the progression of contraction. In this context, it would make sense that the frequency (or the amount) of tendon organ discharges does not increase linearly with muscle force, because if it did, difficulty in recruitment of motor units would increase with increasing efforts. Sensitivity of tendon organs for small changes in muscle force might allow permanent adjustment of autogenetic inhibition to variations of motor output. Although this simple view has not been disproved so far, it appears oversimple and unlikely to account by itself for the intricate processes of motor control. Recent studies have revealed that the operation of the spinal circuit mediating autogenetic inhibition, now termed nonreciprocal inhibition, is much more sophisticated. The effects of tendon organs on motoneurons are assisted by a variety of other inputs converging on common interneurons and controlled by the same supraspinal centers that issue the contraction commands. This again makes sense in view of the almost infinite repertoire of motor acts involving various numbers and types of muscles (see Ref. 214), as does the widespread distribution of Ib effects, obviously required for coordination of limb movements (see Ref. 127). Depending on the specific patterns of motor command, Ib afferent action may be dispatched in different pathways together with appropriately selected input from other receptors. Human studies have provided enlightening examples of the modulation of Ib effects during voluntary contractions. Further studies are needed to fully understand the cooperation of information from tendon organs and other muscle, skin, and joint receptors in force feedback and control of muscle contraction. Other directions in which additional investigations would be necessary include the function of trisynaptic Ib inhibitory pathways to motoneurons and their possible convergence with pathways of presynaptic inhibition. Little is known on the excitation of antagonist motoneurons by Ib afferents, and there is still some uncertainty about the actions of Ib afferents from flexor muscles of the cat hindlimb. Finally, it might be recalled that nothing is known of neurotransmission in Ib pathways. Command of muscle contraction implies a series of choices, which muscle, which type of motor unit, how many units, and what activation frequencies, whereas coordination requires choices about participation of synergic muscles, close or distant, and inhibition of antagonists. Most of the decisions are made at levels higher than the spinal cord, and since information from tendon organs is forwarded to the cerebellum and cere-

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bral cortex, it might take part in higher steps of motor control by pathways and mechanisms that remain to be established. Exploration in cerebellum and brain will most certainly reveal further examples of convergence of messages from various origins in the pathways processing Ib inputs. This should not be taken as an indication that the information provided by tendon organs has no specific function but rather that a precise control of muscle contraction, whether reflex, automatic, or voluntary, requires the integration of data available from the largest possible range of sources. I am deeply indebted to Prof. Y. Laporte for constant support and careful critical reading of this review. Thanks are also due to Dr. E. Jankowska, Prof. A. Lundberg, Prof. E. Pierrot-Deseilligny, and Dr. D. Zytnicki for helpful comments and advice.

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Responses of isolated Golgi tendon organs of the cat.

Golgi tendon organs in the proximal tendon of sheep extraocular muscles.

The distribution of Golgi tendon organs and muscle spindles in masseter and temporalis muscles of the cat.

Connective-tissue macromolecules in Golgi chicken tendon organs and at their interface with muscle fibers and adjoining tendinous structures.

Functional Overload Enhances Satellite Cell Properties in Skeletal Muscle.

Ionic currents in mammalian fast skeletal muscle.

Heterogeneity of motor units activating single Golgi tendon organs in cat leg muscles.

A simple in vitro preparation of mammalian tissue exhibiting properties of slow tonic skeletal muscle [proceedings].

The response of Golgi tendon organs to single motor unit contractions.

The responses of Golgi tendon organs to stimulation of different combinations of motor units.

Glutamine transport and metabolism in mammalian skeletal muscle.

Passive force generation and titin isoforms in mammalian skeletal muscle.

Carbonic anhydrase activity in mammalian skeletal and cardiac muscle.

An active learning mammalian skeletal muscle lab demonstrating contractile and kinetic properties of fast- and slow-twitch muscle.

Functional Properties of Dendritic Gap Junctions in Cerebellar Golgi Cells.

Cellular and molecular diversities of mammalian skeletal muscle fibers.

Functional adaptation of tendon and skeletal muscle to resistance training in three patients with genetically verified classic Ehlers Danlos Syndrome.

Potentials in mammalian skeletal muscle from collagenase-treated tissue.

Detection of fusion events in Mammalian skeletal muscle.

Inward rectifier potassium currents in mammalian skeletal muscle fibres.

Hydroperoxide metabolism in mammalian organs.

Responses of tendon organs in a lizard.

Passive skeletal muscle excursion after tendon rupture correlates with increased collagen content in muscle.

Functional and metabolic consequences of skeletal muscle remodeling in hypothyroidism.