Electrical interaction between motoneurons and afferent terminals in cat spinal cord.

JOURNALOF NEUROPHYSIOLOGY Vol. 42, No. 3, May 1979. Printed in U.S.A.

Electrical Interaction Between Motoneurons Merent Terminals in Cat Spinal Cord D. R. CURTIS,

D. LODGE,

AND

and

P. M. HEADLEY

Department of Pharmacology, John Curtin School of Medical Research, Australian National University, Canberra City, ACT, 2601, Australia

PAD, are not generated in lumbar dorsal roots of the cat by stimulation of ventral 1. The electrical threshold of the terminaroots (1, 17), although high-intensity stimutions of single group Ia and II afferent lation of sacral ventral roots produced sacral fibers was transiently reduced by the antidromic discharge of the initial segment of dorsal root potentials (23). The technique introduced by Wall (27), spinal motoneurons in the cat. whereby afferent fibers are stimulated elec2. This depolarization of the terminals of trically within the cord, provides a direct afferent fibers known to synapse on motoneurons confirms previous observations of method for measuring excitability changes induced in Ia afferent fibers and terminals antidromic electrical interaction between by prior stimulation of ventral roots. Pubthese structures. lished results of such experiments are not in complete agreement. In Wall’s (27) INTRODUCTION original study, antidromic stimulation of Although the synapse between group Ia motoneurons produced no detectable changes afferent fibers and spinal motoneurons in in the excitability of group Ia terminations in the ventral horn. More recently, “minor the cat is frequently accepted on morphological and physiological grounds as a changes” in excitability, both “facilitatory and inhibitory” were reported about 1 ms paradigm of chemical excitatory transmission (11), the transmission process may not after ventral root stimulation and lasting be solely chemical in nature. The inability 0.3 ms (16), confirming similar observations to measure a “reversal” potential for the of “excitatory, inhibitory and both excitainitial component of the excitatory post- tory and inhibitory effects” on single synaptic potential has led to the proposition presynaptic fibers, synchronous with the that transmission may be in part electrotonic, recorded motoneuron antidromic field poextracellular electrical coupling presumably tential (10). depending more on the area of synaptic There are major difficulties, however, in contact than on the width of the synaptic studies of this type. Changes in afferent cleft (12,24,29). Such coupling may also be terminal excitability induced by motoneuron important in the depolarization of group Ia firing may be small and detectable only by terminations by antidromically discharging measuring the threshold close to the fiber alpha-motoneurons, which has been claimed termination. On the other hand, the presence (6-Q not confirmed (16), and reasserted of a stimulating microelectrode in this region (9). This depolarization led to the generation may damage or destroy motoneurons, thus. of antidromically conducted impulses in Ia reducing the chance of detecting antidromic afferent fibers of lumbar dorsal roots in the coupling. Failure or variability of the anticat, especially when superimposed on pri- dromic invasion of motoneurons may, in mary tierent depolarization (PAD) produced fact, account for some of the different obby orthodromic impulses in other afferents. servations mentioned above. Consequently, There are other reports, however, that a study has been made of threshold changes dorsal root potentials, also a measure of at the terminations of single spinal afferent SUM

MARY

AND

CONCLUS

IONS

0022-3077/79/0000-OOOO$O1.25 Copyright

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Society

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636

CURTIS,

LODGE,

fibers associated with the antidromic discharge of individual motoneurons in the close vicinity. METHODS

The experiments were carried out in lumbar segments of 11 cats anesthetized initially with pentobarbital sodium (35 mg kg-l, ip) and maintained as required with l-3 mg kg-l intravenously. The cord was transected at the thoracolumbar junction, exposed tissues were covered with liquid paraffin, the temperature of which and also that of the animal, was maintained at 37-38OC. Gallamine triethiodide was not used in this investigation and all animals were respiring spontaneously. In all experiments peripheral muscle nerves were sectioned as far distally as possible, subdivided into small bundles, and mounted on bipolar platinum electrodes for stimulation or for the monophasic recording of action potentials. The nerves included those of the medial and lateral gastrocnemius-soleus (M and LG), plantaris (PL), and flexor digitorum longus (FDL) muscles. In seven cats, ventral roots (VR) L,, S1, and S, were cut proximal to the dorsal root ganglion and mounted on stimulating electrodes well clear of dorsal roots and accumulations of cerebrospinal fluid. In these animals the nerves to posterior biceps semitendinosus (PBST) muscles were cut and mounted on stimulating electrodes so that the terminals of extensor muscle primary afferents could be depolarized synaptically. In the other animals, ventral roots were left intact and dorsal roots (DR) L7, S1, 2, and 3 were transected close to the appropriate ganglia. That of L, was divided into two or three bundles, which together with the S, dorsal root were mounted separately on bipolar recording electrodes. This type of preparation, in which antidromic volleys were initiated in small bundles of motor nerves peripherally, was used in order to reduce the number of motoneurons activated antidromically at a given recording site. Motoneurons were located within the ventral horn using 3.6 M NaCl-filled glass microelectrodes of tip diameter l-2 pm, resistance 2-5 Ma. These electrodes were then used to stimulate primary afferent terminations having electrical thresholds of 0.3-2 PA (negative pulse, 0.12-0.3 ms duration, 10 Hz) and located within motonuclei. The frequency of antidromically conducted impulses in a single fiber, recorded from either a dorsal rootlet or peripherally from a subdivided muscle nerve and selected by a gated window discriminator, was maintained at 5 Hz by a feedback circuit, which compared the stimulating (10 Hz) and response frequency and l

l

AND

HEADLEY

regulated the amplitude of the stimulating pulse. The amplitude of the pulse maintaining a firing index of 50% thus provided a direct measure of fiber threshold, and changes in pulse amplitude were monitored continuously on a paper recorder. Conditions were generally sufficiently stable to allow the detection of changes as small as 2%, and each point in Fig. 1 represents a mean value of the altered threshold over a period of at least 7 s, i.e., more than 70 trials. In some experiments the recording and stimulating electrode was the center 3.6 M NaCl-filled barrel of a seven-barrel micropipette, and the effects were determined on fibers of the balanced electrophoretic administration of sodium and chloride ions, GABA and chloride, and L-glutamate and sodium (see Ref. 5). RESULTS

The majority of the muscle afferent fibers studied were presumably excited near their terminations in the vicinity of motoneurons. The criteria for near-terminal excitation include proximity to motoneurons, a relatively low ratio between threshold currents and those which produce “anodic” block, a reduction in threshold (by as much as 40%) by prior tetanic (four volleys, 320 I-Iz, 2-3 x threshold) stimulation of the PBST nerve 40 ms earlier, and the reduction in threshold induced by electrophoretic GABA and L-glutamate (5). Although the majority had conduction velocities to the periphery within the group I range (70- 100 me s-l), and presumably were group Ia fibers (28, 30), some were group II fibers (24-70 ma s-l), which also excite motoneurons monosynaptically (13, 18, 20, 25). Identification on the basis of conduction velocity was less precise, however, when recording from dorsal roots. Changes in fibers threshold

In the first six animals used in this investigation, the thresholds of very few fibers were modified by prior stimulation of the segmental ventral root (VR). Reductions of the order of 2-7% (mean 3.9%) were observed with 19 of 104 fibers tested, over intervals from 0.2 to 0.8 ms after the ventral root stimulus. With one fiber, however, which was of group II conduction velocity, there was a maximum change of almost 25%, at an interval of 0.3 ms. Increases in fiber threshold were never observed and antidromic discharges were never recorded


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FIG. 1. Changes of the threshold of primary afferent terminals associated with the antidromic firing of the initial segment of motoneurons. A : upper: antidromic potential recorded near a motoneuron in response to a ventral root stimulus at an intensity of 62.5 on an arbitrary scale (arrow). The dotted line is the potential evoked by a just-subthreshold stimulus (intensity 60). Voltage calibration: 2 mV. Lower: change in the electrical threshold of an FDL group I afferent termination excited by a ~-PA 0.12-ms (horizontal bar) pulse (10 Hz); l , VR stimulus intensity 62.5; n , VR stimulus intensity 60. Ordinate: change in threshold as a percentage of the control pulse amplitude. Abscissa: ‘time in milliseconds after the VR stimulus. B: upper: antidromic potentials recorded extracellularly (EXC) and intracellularly (IC) from a motoneuron in response to stimulation of the medial gastrocnemius nerve (stimulus intensity 35). The dotted line indicates the field potential generated by a just-subthreshold stimulus (intensity 34). Voltage calibrations: 0.4 and 4 mV. Lower: change in the electrical threshold of the termination of a primary afferent fiber in the S, dorsal root excited by a O.&PA, 0.2-ms pulse (10 Hz); l , nerve stimulus intensity 35; n , nerve stimulus intensity 34. Ordinate: as for A. Abscissa: time in milliseconds after the peripheral antidromic stimulus.

from afferent fibers in the absence of electrical stimulation of terminations, as have been reported previously (7, 10). All of the fibers that were depolarized were close to motoneurons, as indicated by the amplitude of extracellularly recorded antidromic field potentials, and it was apparent that the largest changes in excitability occurred when relatively large potentials were recorded from a single motoneuron. No fibers were depolarized when antidromically evoked field potentials were relatively small, and some fibers were depolarized only when antidromic invasion of motoneurons was facilitated by an earlier orthodromic volley originating in another muscle nerve, such a volley itself not altering the fiber threshold. Under these conditions, however, not every primary

afferent in the immediate vicinity was depolarized. For any one fiber the change in excitability was of an all-or-none nature; specifically the VR stimulus, which was threshold for antidromic invasion of the motoneuron, was also threshold for the effect on the afferent terminal. Furthermore, VR stimuli of greater intensity produced no further change in the excitability of any one fiber. These observations suggest that terminals synapsing only with a particular motoneuron were affected. In these early experiments, fibers were selected primarily on the basis of low electrical thresholds (< 1 PA), rather than on their proximity to antidromically activated motoneurons. Furthermore, with stimulation of ventral roots, even when subdivided, difficulty was frequently experienced in


638

CURTIS,

LODGE,

distinguishing the action potentials of individual motoneurons from field potentials generated by many cells. Subsequently, sites for investigation were chosen primarily on the basis of the recording of action potentials of single motoneurons, a task that was considerably facilitated by stimulating subdivided branches of peripheral muscle nerves, the dorsal roots having been cut. As a result, the number of fibers in which a reduction in threshold was detected was increased -reduction in threshold ranging between 3 and 19% (mean 7.5%) were observed with 17 of the next 31 fibers investigated. Additionally, the use of peripherally originating antidromic volleys enabled the time course of the threshold changes to be correlated more accurately with the potentials recorded near motoneurons, although the type of fiber stimulated within the cord could not be identified precisely because of the relatively short conduction distance within the dorsal rootlets. A particularly clear example is illustrated in Fig. lA of the change in threshold of a group I (79 m s-l) FDL termination induced by stimulation of the ventral root. The all-or-none, negative action potential of a motoneuron had an amplitude of approximately 5 mV. With a just-subthreshold ventral root stimulus, there was no alteration in fiber threshold. When the ventral root stimulus was above threshold for this extracellularly recorded potential, however, the threshold of the fiber was reduced, as plotted in the lower half of the figure. The maximum reduction of 8% occurred when the beginning of the stimulating pulse corresponded to that of the action potential, and the total duration was approximately 0.7 ms but commencing 0.2-0.3 ms before the action potential. With other fibers, and especially when pulses of 0.2 or 0.3 ms were used to determine fiber thresholds, the onset of changes in threshold associated with motoneuron antidromic potentials also preceded these potentials by as much as 0.3 ms. This is shown in Fig. lB, in which the motoneuron (extracellular action potential 2.1 mV) was fired by stimulating one branch of the MG nerve. Following the measurement of the changes in threshold of a fiber recorded in the S, dorsal root (latency 0.85 ms) the motoneuron was impaled, and the intral

AND

HEADLEY

cellular record (IC) gives a more accurate indication of the time at which the antidromic action potential originated. The reduction in threshold began when the stimulus was 0.28 ms before the action potential, with a maximum reduction (9%) 0.2 ms later. As with the fiber of Fig. lA, subthreshold stimulation of the MG nerve failed to alter the excitability of the afferent fiber. The timing of these changes in threshold are characteristic of the results obtained with all other afferent fibers. When relating them to the antidromically evoked potentials recorded near motoneurons, allowance must be made, however, for the latent period of the electrical excitation of fiber terminations by just-threshold stimuli. With the fiber of Fig. 1B , the difference in DR conduction times between impulses initiated by 2x threshold stimulation of the termination (0.2 ms, 1.6 PA) and just-threshold stimuli (0.2 ms, 0.8 PA) was 0.22 ms. With other intraspinal fibers and terminals, this time was as long as 0.34 ms. When latencies of activation of the order of 0.2-0.3 ms are allowed for, the onset of changes in afferent fiber threshold correspond in timing with the earliest phase of the antidromic potentials recorded near motoneurons, and the duration of the change s are similar to those of these potentials. Nature

of antidromic

potentials

Potentials recorded extracellularly in the vicinity of antidromically activated motoneuron may be complex, depending on whether all three regions (axon, initial segmerit, somadendrites) produce action potentials, and the location of the electrode in relation to them (26). Further complexity arises from membrane damage by the electrode, and especially if “giant” extracellular potentials are recorded by an electrode impinging on the membrane. In general, however, two major components of antidromically evoked potentials are recognized, that produced by the initial segment (IS) and that subsequently generated by the somadendritic (SD) region. These are most readily distinguished by using two ant idromic volleys , the second timed so that the SD membrane is refractory (2). In the present investigation it was rare to record near single motoneuron negative extracellular potentials that had stepped


MOTONEURON

PRESYNAPTIC

rising phase and that could be fractionated into IS and SD components by the two-volley technique. More often the rising phase of the all-or-none potentials showed no evidence of a discontinuity (see for example, Fig. 1A ); occasionally there was a biphasic peak or a hump on the falling phase. That these potentials were generated by the initial segment was further suggested by the response to the second of two stimuli, there being either no change in shape or a loss of the later component at intervals as short as 1 ms. The possibility that the motoneurons were damaged by the microelectrode, which of necessity was required to be in the close vicinity of afferent terminals on somatic and dendritic membrane, complicates this Nevertheless, extracellular investigation. records from eight neurons indicated that an IS potential was adequate to modify terminal excitability. The potentials illustrated in Fig. 1 recorded near two motoneurons were IS in nature, as was the intracellular potential of Fig. 1B. Satisfactory records were obtained from only one motoneuron for which there was a discontinuity on the rising phase of the antidromic potential, and only an IS potential was generated by a second volley at an interval of 9 ms. There was, however, the same reduction (5-6%) in the threshold of a caudal L7 DR fiber as when the full IS-SD sequence occurred. With only one motoneuron did invasion of the SD segment appear necessary for the reduction in the threshold of an afferent termination. When a VR stimulus, which evoked an IS-SD potential and reduced the threshold of a termination, was preceded by a stimulus 9 ms earlier, only an IS potential was recorded and there was no concomitant reduction in the fiber threshold. Movement of the electrode from the vicinity of both the fiber and the motoneuron prevented full analysis of this rare event. DISCUSSION

These results are in agreement with previous observations that antidromically propagating impulses in the ventral roots of lumbar segments of the cat spinal cord can transiently lower the electrical threshold of afferent fibers known to synapse monosynaptically with motoneurons. The reduction in threshold indicates a depolarization

DEPOLARIZATION

639

of terminals, and changes in fiber threshold of the opposite direction were never observed. The amplitude of extracellularly recorded antidromic potentials suggested that depolarized fibers were close to motoneurons, possibly within 300-500 ,um of the soma (see Ref. 22), although not all fibers in the immediate vicinity of a motoneuron were affected. The depolarization, which reduced fiber thresholds by as much as 25% but generally much less than this, lasted 0.60.7 ms, and its onset coincided with that of the antidromic invasion of the initial segment of motoneurons. Furthermore, there appeared to be no requirement for a somadendritic component of the antidromically activated potential. Since changes in threshold of the order of 2% could be detected, the all-or-none association of the change in threshold of a termination with the antidromic discharge of a single motoneuron suggests that the length constant of preterminal fibers is such that there is insignificant electronic spread of membrane potential changes from one branch to another. Although complications introduced by the presence of the recording/microstimulating electrode near motoneurons cannot be evaluated, these observations suggest that the transient depolarization of primary afferent terminals (groups I and II) synapsing on motoneurons results from the extracellular flow of current generated by the propagation of an action potential into the initial segment. For approximately 0.6 ms, the somadendritic membrane is a “source” of current which, by flowing outward across this membrane, through the presynaptic membrane of apposing afferent terminals, and thence outward through the rest of the terminal and adjacent nodes, could lower the electrical threshold of these structures. Such an explanation presupposes reasonably low-resistance coupling between motoneurons and afferent terminals, also a requirement for electrical coupling in the reverse direction (12,24). Depolarization of terminals by extracellular current flow was also proposed by Decima (6) and Decima and Goldberg (9) to account for antidromic depolarization of afferent terminals in the cat, although the present more direct evaluation of such depolarization suggests that, rather than extracelluar current produced by the antidromic firing of motoneurons, the


CURTIS, LODGE,

640

currents are those generated by invasion of the initial segment. An electrical interaction between motoneuron dendrites and afferent fiber terminal arborizations has also been proposed as the basis for the short-latency ventral root-dorsal potentials recorded from the frog spinal cord in vitro treated with gallamine triethiodide (14). Failure to demonstrate changes in terminal threshold during the SD phase of antidromic invasion may suggest that electrical coupling between the motoneuron SD membrane and apposed terminals is relatively insignificant. A complicating factor would be whether or not membrane subsynaptic to afferent terminals participates in the conductance changes and current flow associated with somadendritic action potentials. Additionally, it is also possible that while extracellular current flow associated with invasion of the SD membrane by an action potential would hyperpolarize terminals synapsing on it, low-resistance electrical coupling between the membrane and the terminals would depolarize the latter structures, such effects tending to cancel. On the other hand, damage by the electrode may have prevented the antidromic action potential from exciting the SD membrane of the motoneurons investigated. In this regard it is significant that Decima and Horn (10) observed biphasic alterations in the excitability of some single presynaptic fibers associated with the antidromic discharge of motoneurons: a reduced threshold of similar time course to those illustrated in the present paper being followed by an increased threshold of equal or smaller magnitude and variable duration. It seems probable that in these earlier experiments damage to motoneurons was less than in the present investigation as afferent fibers rather than presynaptic terminals were stimulated within the cord (E. Decima, personal communication). Combined intracellular recording from a motoneuron with extracellular stimulation of primary afferent terminals on it appears necessary to resolve these questions, which may be of significance

AND HEADLEY

to the nature of orthodromic coupling between afferent terminals and motoneurons. Elevation of the extracellular potassium concentration as a consequence of the antidromic firing of motoneurons seems an unlikely factor reducing the threshold of afferent terminatons. Repetitive (100 Hz) VR stimulation produced very little increase in “extracellular” levels of potassium ion activity as measured by means of a potassiumspecific microelectrode located in the ventral horn (19) and, in the present experiments, VR stimulation at 100 Hz produced no greater change in excitability than did stimulation at 10 Hz. A direct depolarizing interaction has been demonstrated between neighboring lumbar motoneurons (15, 2 l), which may be either electrical or involve excitatory recurrent collaterals between synergistic motoneurons (3, 4, 12). The latency of the interaction and the apparent insensitivity of motoneurons to acetylcholine probably excludes this latter explanation. The very brief duration of the depolarization of terminals that was demonstrated, and their relationship to the IS rather than to the SD segment of motoneurons, raise doubts as to the physiological significance of antidromic depolarization of primary afferent terminals as a method for influencing monosynaptic excitation of motoneurons by modulation of transmitter release. Such a brief negative feedback mechanism would seem relatively unimportant in view of the rather low-frequency response of motoneurons, although brief changes in the electrical threshold of terminals may not necessarily reflect the time course of changes in transmitter release induced by extracellular current flow. ACKNOWLEDGMENTS

The authors are grateful to Professor E. Decima and Dr. S. Redman for comments on this manuscript, and to Mrs. P. Searle for skilled technical assistance. P. M. Headley held a Queen Elizabeth II Fellowship. Received 20 June 1978; accepted 14 December 1978.

in final form

REFERENCES 1.

BARRON, D. H. AND MATTHEWS, B. H. C. The interpretation of potential changes in the spinal cord. J. Physiol. London 92: 276-321, 1938.

J. S., CURTIS, D. R., AND ECCLES, J. C. The interpretation of spike potentials of motoneurons. J. Physiol. London 139: 198-231, 1957.

2. COOMBS,


MOTONEURON

PRESYNAPTIC

S. AND KELLERTH, J.-O. A morphological study of the axons and recurrent axon collaterals of cat sciatic a-motoneurons after intracellular staining with horseradish peroxidase.

3. CULLHEIM,

J. Comp. 4. CULLHEIM,

5.

6.

7.

8.

Neurol. 178: 537-558, 1978. S., KELLERTH, J.-O., AND

CONRADI,

S. Evidence for direct synaptic interconnections between cat spinal cu-motoneurons via the recurrent axon collaterals: a morphological study using intracelluar injection of horseradish peroxidase. Brain Res. 132: l-10, 1977. CURTIS, D. R., LODGE, D., AND BRAND, S. J. GABA and spinal afferent terminal excitability in the cat. Brain Res. 130: 360-363, 1977. DECIMA, E. E. An effect of postsynaptic neurons upon presynaptic terminals:Proc. Natl. Acad. Sci. U.S.A. 63: 58-64, 1969. DECIMA, E. E. AND GOLDBERG, L. J. Centrifugal dorsal root discharges induced by motoneurone activation. J. Physiol. London 207: 103- 118, 1970. DECIMA, E. E. AND GOLDBERG, L. J. Antidromic electrical interaction between alpha motoneurons and presynaptic terminals. Brain Res.

57: l-19, 9. DECIMA,

1973.

E. E. AND GOLDBERG, L. J. Motoneuronpresynaptic interaction in the spinal cord of the cat: rebuttal to a denial. Brain Res. ,110: 387391, 1976. 10. DECIMA, E. E. AND HORN, R. Time course of motoneuron-presynaptic interaction in the cat spinal cord. Intern. Congr. Physiol. Sci., 25th, Munich,

Sci.

137: 473-494,

135- 150, 1978. 15. GOGAN, P., GUERITAUD, J. BOSAVIT, G., AND TYC-DUMONT,

P., HORCHOLLES. Direct excitatory interactions between spinal motoneurones of the cat. J. Physiol. London 272: 755-767, 1977. 16. GUTNICK, M., RUDOMIN, P., WALL, P. D., AND WERMAN, R. Is there electrical interaction between motoneurons and afferent fibers in the spinal cord? Brain Res. 93: 507-510, 1975.

E., AND LINDSTR~M,

S.

London

215: 613-656,

1971.

18. KIRKWOOD, P. A. AND SEARS, T. A. Monosynaptic excitation of motoneurones from muscle spindle secondary endings of intercostal and triceps surae muscles in the cat. J. Physiol. London 245: 64-66P, 1975. 19. KRfZ, N., SYKOVA, E., UJE~, E., AND VYKLICKY, L. Changes of extracellular potassium concentration induced by neuronal activity in the spinal cord of the cat. J. Physiol. London 238: l- 15,1974. 20. LUNDBERG,

A., MALMGREN,

K., AND SCHOMBURG,

E. D. Comments on reflex actions evoked by electrical stimulation of group II muscle afferents. Brain

Res.

122: 551-555,

1977

21. NELSON, P. G. Interaction between spinal motoneurons of the cat. J. Neurophysiol. 29: 275287, 1966. 22. NELSON,

potential

P. G. AND FRANK, K. Extracellular fields of single spinal motoneurones.

J. Neurophysiol. 23. NIECHAJ, A.,

27: 913-927, 1964. LUPA, K., AND OZOG,

M. Dorsal root potentials evoked by stimulation of ventral roots in the lower sacral cord of the cat. Brain Res.

137: 356-360, 1977. 24. RALL, W., BURKE, R. P. G., AND FRANK,

E., SMITH, T. G., NELSON, K. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J. Neurophysiol.

25.

30: 1169- 1193, 1967. STAUFFER, E. K., WATT, D. G. REINKING, R. M., AND STUART,

D., TAYLOR, A., D. G. Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents. J. Neuro-

physiol. 39: 1393- 1402, 1976. 26. TERZUOLO, C. A. AND ARAKI,

T. An analysis of intra- versus extracellular potential changes associated with activity of single spinal motoneurons.

1976.

Fu, T. C. AND SCHOMBURG, E. D. Electrophysiological investigation of the projection of secondary muscle spindle afferents in the cat spinal cord. Acta Physiol. Stand. 91: 314-329, 1974. 14. GALINDO, J. AND RUDOMIN, P. The effects of gallamine on field and dorsal root potentials produced by antidromic stimulation of motor fibres in the frog spinal cord. Exp. Brain Res., 32:

13.

H., JANKOWSKA,

Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents. J. Physiol.

1966.

12. EDWARDS, F. R., REDMAN, S. J., AND WALMSLEY, B. The effect of polarizing currents on unitary Ia excitatory post-synaptic potentials evoked in spinal motoneurons. J. Physiol. London 259: 705723,

17. HULTBORN,

1971.

11. ECCLES, J. C. The ionic mechanisms of excitatory and inhibitory synaptic action. Ann. N.Y. Acad.

641

DEPOLARIZATION

Ann. N.Y. Acad. Sci. 94: 547-558, 27. WALL, P. D. Excitability changes

terminations

1961.

in afferent fibre and their relation to slow potentials.

J. Physiol. London 142: 1-21, 1958. 28. WATT, D. G. D., STAUFFER, E. K., TAYLOR, A., REINKING, R. M., AND STUART, D. G. Analysis

of muscle receptor connections by spike-triggered averaging. 1. Spindle primary and tendon organ afferents. J. Neurophysiol. 39: 1375- 1392, 1976. 29. WERMAN, R. AND CARLEN, P. L. Unusual behavior of the Ia EPSP in cat spinal motoneurons. 30.

Brain Res. 112: 395-401, WILLIS, W. D., NAN&,

1976.

R., AND RUDOMIN, P. Excitability changes in terminal arborization of single Ia and Ib afferent fibers produced by muscle and cutaneous conditioning volleys. J. Neurophysiol. 39: 1150- 1159, 1976.


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