Ncaroscke Printed in

Vol. 46,

No.4, pi. -,

0306422p2 55.00+0.00 ~lw-~plc

1992

CirmtBritain

IBItO

MOVEMENT-DEPENDENT AFTER-EFFECTS IN THE FIRING OF THE SPINDLE ENDINGS FROM THE DE-EFFERENTED MUSCLES OF THE CAT HINDLIMB A. I. KIXTYUKOV ad

V. L. -Y

A. A. Rogomoktz Institute of Physiology, Uhminkn Academy of Scknces, Rogomoletz str. 4, 252601 GSP, Rkv 24, U.S.S.R. ~~muTclcrpindlererrdionsevolralbytbc~~trolled~~inthcmuscklen%hor bad weze studied on the de-dfemntd muscks in experiments on cats under Nembutal EMU&&. The activity of 39 primary and 10 mcondary endings of the muscle spindles from four hindhmb ~muccks:sdaqphntariqh~udmedinitatedsof~trocnani~~been~rdcd during aervocoDtfoucd changes in made kmgtb (Uxmtrol) or external load (P-coMrol). Slow linear racipoatin(l (h+gular) signals and thek mod&&on with fixation of the controlled parameter at the comma&forthemusckstMcherThesteady !3amekvelatforwudaudreWrsephaseawereusedas ~gn~in~ard~eading~~tionofmude~orexternalloadwacshown TEelIlingrateswere tobestronglydepemkntonthedim&mofpmvi0uachangesinthese~. alwayshigheraRerpmxdingk@asing(Ioad&)andbweraI&sh0rta@([email protected] ~~intbertr_rdvfirinsobrphdlcmdinsattberamekvelof~ntrolled~rcouldbe asmuch~15-#)p~.s.The~depmdsnaofthcPpindle~gfiriagontbepnstbistoryoftbe vt&pemkut after-etkcts. Two hinds of moxmentdepemknt muademovenmutwasdenotedaa an be obsen& (1) the movement&pendent ones being aIter&ectsintheIkIngoftheapindkaldiugs with the conditioning fusiitor stimulation and studiaIinthepn?sentwork,aud(2)thoseaumeued describedehxwimm.lheircommon comiected tith the hystemtkal (thixotropic) moWmentdepemknt after-effects in L- and comes&d with a resemblance of the length-tiring rate [F(L)] and rotating movements. Roth hinds of loops ~rd-hriag~teF01h~~~dmingIecip were in a doch-wise dime&n, Thor m in normahmd form showed that F(L) kops were always

extaaot

mty vectors were introduced to analyse quantitatively the hysmretical etfcdsinthespindlefiringmdthehrrrhfiontothemuackh~~spropcr.Un~ntyvedorscoMed the points of equal load (isotonic PllocrtaiELty mctors) and equal kngth (isometric unuxtamty vectors) on F(L) and P(P) lo0ps w. The projectbns of both uncerminty vectors onto the Y-axis give the rate umxtainty coin&l& irt sign for both cases, whereas their projections onto the X-axis differ in sign, being positive for kometnc lllloc~lllty vectors (the tension uxertainty) and negative for isotonic ety W&Jm We rcnsta m=rtaiW). the greater the mtio between hyatm&al aItor+&cts (static errors in the propri0ceptor lking and in the ~)_.Sertisticalanrlysitoftbeobtaincdwithl~and~~tionshowcdtbatin EYm and mumdary endings kometrk unartainty vectors were closer to 90” as compared to isotonic mty vectors. The awaged angles were 60.3 f 3.3” (primaries) and 70.0 f 3.9” (secondarics) for kometrk mty vectom, and 130.1 f 4.2” @rimarks) and 130.0 f 4.6” (secondaries) for isotonicunartrintyvedors.ThuqtbtRtiobctmenthestaticmoninthcspin~tndingfiringandthe hysmretkal ummtainty in mkbrulial state of muack is higher for the length tracking by these proprioceptors as compamd with the load trachmg.

In 1951 Hunt and coworkers showed a per&tent rise innxtctionaoftheapindkprimaryuxI.&saRcra

brief period of fusimotor stimulati~n.~ It was shown that fusimotor stimulation was f&wed by a long-lasting incEase in thir background activity. Later, Brown et ol.” studied, in detail, such [email protected] showed, in pa&ular, the post-stimulation

Abbrmiolioru:

heighten-

D, diecriminotor

puke? DT* “Mt v& ium; F, instantaneous rate; IMUV, rsome& uncutam vector; ITUV, isotonic uaartahty vador; L. Iclyth; P, load. 989

ing of the initial bursts in the firing evoked in primary endings by a standard muscle kqthcnhg and supposedthattheseafter4ectswmmainlymechanical in origin. Fuaimotor activation of intrafuaal fibres seems to increase the number of stable cross-bridges between actin and myosin myohncnts. Being rather persistent in isometry, these bounds, at the same time, are easily destroyed by muscle kngthening for several millime&s. Recently, the formation and destruction of the aReu-&‘ects were studied by using more and more complex combinations of mechanical stimuli with conditioning and testing intraful stimulation that

990

A.I.

KOSTYUKOV

and V. I,,

led to more general hypotheses about these processes.5-7~‘1.‘4~27.30 In all these studies, mechanics of intrafusai muscle fibres was considered as being of paramount importance for the understanding of the after-effects in the firing of the spindle endings. It seems that the main attention should be primarily focused on the muscle thixotropy, or hysteresis. Thixotropy and hysteresis are, in a way, overlap ping concepts dealing with almost the same muscle properties. The thixotropy is usually determined by the dependence of muscle stiffness or viscosity on the immediate past history of the movement.2i The hysteresis, on the other hand, is determined through the well-known length-tension loops recorded during slow reciprocating changes in muscle length.32 In so far as the hysteresis occurs even during very slow movements, it must be treated as non-linear statics of the muscle.‘? Besides the hysteresis evoked by changes in the muscle length or load, similar hysteretical loops might be registered under isometric or isotonic conditions during cyclic changes in the efferent stimulation rate.‘3F’8*28Hence, two kinds of muscle hysteresis can formally be considered and both of these are characterized by rather powerful and longlasting after-effects. Muscle generates higher (lower) tension under isometric conditions when it was lengthened (shortened) prior to the length ~xatio~,l,4,34,35 whereas under isotonic conditions two distinct steady-state lengths are also set, depending on the past history of movement.‘? Differing from these after-effects, the second kind can be observed during two oppositely directed changes in the rates of the efferent stimulation and their subsequent fixation at the same level. Using this type of stimulation two different steady values of tension or length were inevitably correspondingly recorded under isotonic and isometric conditions.i3~i8 Hysteresis in intrafusal muscle fibres might be considered to underlie the well-pronounced hysteresis depending on the rate of the spindle firing and muscle length. This kind of hysteresis was shown to be present in the activity of primary and secondary endings. 22Supposing an analogy between mechanical properties of extra- and intrafusal muscle fibres, one may expect the existence of two distinct kinds of hysteresis and the corresponding after-effects in the firing of spindle endings. If this is the case, the abovedescribed fusimotor after-effects in the spindle firing should belong to the kind of hysteresis in intrafusal fibres which is linked with slow changes in the intensity of their activation. On the contrary, similar after-effects might be expected for the spindle hysteresis connected only with passive muscle movement without fusimotor drive. To distinguish between these after-effects they will be referred to further as the movement-dependent ones. It should be pointed out that in the previous studies concerned with the after-effects in the activity of the spindle endings not only were fusimotor after-effects described but also,

CHERKASSKY

to some extent, the movement-dependent

ones.i~6~2’ Nevertheless, this kind of after-effect was not explored systematically considering, in particular, a lack of comparative studies between the oppositely directed conditioning movements. In the present study we compared the after-effects connected with both directions of the preceding movements. Using the servo-controlled test changes in muscle length or load, an attempt was made to analyse the movementdependent after-effects in the firing of primaries and secondaries from the de-efferented muscles of anaesthetized cats. The spindles under study were deprived of the fusimotor activation.

EXPE~MENTAL

PROCEDURES

Experiments were carried out on 28 cats 2.9-3.8 kg in weight, anaesthetixed with Nembutal (initial dose 45 mg/kg i.p. with additional i.v. injections if needed). The soleus, plantaris, lateral and medial heads of the gastrocnemius muscles of a hindlimb were separated from the surrounding tissue and their tendons were cut and sewed to iron hooks to connect them with the servo-controlled muscle stretcher. AU the limb nerves except those going to the test muscles were cut. Laminectomy was performed in the region of the lumbar enlargement of the spinal cord. L&i2 dorsal and ventral roots were cut at points where they left the spinal cord. The animal was fixed securely in a stereotaxic frame; the tibia and knee joint were also rigidly fixed. Muscles under test and nerves were piaced in the bath formed from shrouding skin and tXed with pan&in oil heated to 38°C. A similar bath was made around the exposed spinal cord. Rectal temperature was maintained at 37-38°C. Afferent fibre activity was recorded only if arterial pressure did not fall below 90 mmHg. Spike activity from proprioceptors in the test muscles was recorded in fine filaments of Ls-S2 dorsal roots by bipoiar Ag-AgCl, electrodes. Identification of units was carried out by a standard technique in&ding an analysis of the reactions to isometric twitches evoked by the stimulation of the muscle nerve. Primary and secondary endings were distinguished by conduction velocities; the value of 72 m/s served as the boundary. Mechanical stimulation ~rvo~n~oiied powerful linear motor of a loud-speaker type was used as the muscle stretcher. External load or muscle length could be precisely controlled by the stretcher. The load (or muscle tension) was measured by semiconductor strain gauge resistors; muscle length was registered by means of a precision potentiometric transducer. The signals were directed to the recorders and at the same time served as feed-back signals for the servo-system. When the stretcher was connected to a standard elastic load with a stiffness of 50 N/mm, the time constants of the force and length transients did not exceed 60ms in both of the servo-controlled regimens. The compliance of the stretcher itself was 0.025 mm/N. Commands to the stretcher were issued by two special signal generators. It should be pointed out that the forces developed by passive muscles under their maximal physiology stretching are not large, consisting for soleus of about OS-1 N.” Loading the muscle within this range, it was difficult to achieve steady and well-reproducible reactions of the spindle endings, provided that rather complex input signals for the stretcher were used. Therefore, for testing, we had to use heavier loads consisting of 5-g N for soleus and up to It%15 N for other mu&es studied. This allowed us to obtain

991

After-effects in muscle spindle activity

r

L-LsN /

I/-y

L--d-

II

Ill

11

225mm

2s

Fig. 1. Reactions of the spindle primary ending from medial gasttocnemius muscle to the controlled changes in the muscle length. The following records are presented: spikes after discrimination (D), ins~n~~~us rate of firing (F), muscle load (P) and length (L). in A the muscle was initi~y stretched for 6.5mm over its resting length. The records in A are continued in B, where muscle was stretched additionally (marked with asterisk). The phases of the length fixation in the double trapezium are denoted by I, II, III. The averaged rates of firing calculated within shown intervals are indicated above the bars denoting the intervals of the averaging.

stable, high rate (up to 5Op.p.s.) firing of the spindle endings. At the same time such loads were still insticient to damage the muscle and spindle under study. In each experiment the muscles were never stretched more than 12-14mm above their resting length. The absence of any damage during this procedure was proved by comparing the isometric twitch reactions of both muscle and spindle ending before and after every mechanical test. These reactions were evoked by siugle pulse nerve stimulation, whereas the muscle was stretched 2-3 mm above its resting length. Data recording The amplified potentials from dorsal root filaments were discriminated and then directed to a special digital-analogue device to measure the instantaneous rate of firing. Its overall range was 0-1OOp.p.s. with steps of 3.3 p.p.s. After every input pulse the device output voltage was tixed at the level inversely related to the preceding interpulse interval. The output signal of the rate-meter remained unchanged until the next pulse appeared. If no pulse entered during the time interval corresponding to the minimal detectable rate, the zero voltage was set up. To make the rate records in the figures more coherent within long pauses of activity, we changed the rate records slightly by resetting them to zero level (dashed lines) precisely at the moment of last pulse prior to the pause (see, for example, Fig. 1). In addition, when necessary, at periods of steady firing the precise average rates were determined through measuring the number of spikes and the overall time interval of their appearance. Instantaneous rate (F), discriminator pulses (D), length

(L) and load (P) signals were registered by an ink-pen

recorder and simultaneously by a multi-channel taperecorder with frequency modulation (bandwidth &2 kHz at a speed of 19 cm/s). F(L), F(P) and P(L) dependencies were plotted by an X-Y recorder in off-line regimen. RESULTS

To elicit the movement-de~nd~t after-effects in the firing of proprioceptors, the servo-controlled changes in muscle length or external load were used. Two steady levels of firing were compared in the two equal steady states of controlled variable, differing in the direction of the previous change of the variable. The input signal for stretcher obeying this demand can be, for example, produced by modification of a standard linear reciprocating (triangular) signal with fixation at the same level of its forward and reverse phases. This had been produced through summation of the two trapezium signals with the same slopes and different durations so that the more brief trapezium started and ended on the apex of another (double trapezium, DT), Further, we will distinguish the three steady states, or phases (I, II, III) of DT, which correspond to the above-defined fixations of signal. Steady states I and III are equal in magnitude, whereas oppositely directed changes of the signals

992

A. I.K~STYUKOV

and V. L. CHERKASSKY

Fig. 2. Reactions of the spindle primary ending from the sokus muscle to the contrc&ed changes in the externalload.lnitirlbadinAwPsnearlN.Theeumandthc~oftwotnrpszium~swcrc usedasthtcommandsforthem~kstrctcher.RacordrinBarmo~sttartheBsdyroundload increase (indiited by arrow). Note the dil%emncebetween steady-state rates at phases I in both of the test loadings in B.

preceded them, an increase for I and a decrease for III. To eliminate the noticeable dynamic components in proprioceptor reactions we used quite slow changes during ramp phases of the input signals (near 1 s). An example of the primary ending reactions to DT changes in musck length is shown in Fig. 1, reactions of the secondary endings were mainly the same. When comparing the steady levels of firing rates in phases I and III (Fig. IA), it can be seen that the rate was higher when a given isometric state of the muscle was preceded by the kngthe&g as compared with shortening. The di&rence in the caIcuIated average rates (see Experimental Procedures) was as large as 6.2 p.p.s. in this case. At the same time, the further lengthening of the muscle alter its returning to the initial kngth (single trapezium in Fig. 1A) again restored the firing to the rate recorded earlier at phase I of DT. Alter the initial length increase (asterisk in Fig. 1B) the difference between firing rates in phases I and III became even more pronounced (15.2p.p.s.). In most of the spindle endings studied the difference of 15-20 p.p.s. could be obtained with a corresponding choice of DT parameters. By comparing the force and firing rate records both qualitative similarity between them, and similar manifestation of the after-effects, could be seen. Pronounced dynamic changes in muscle tension on passing from movement to isometry seem to affect, in some way, the spindle ending activity. Let us consider, for exampk, the phase III and the transition to it. Quite a long period of silence was usually seen during shortening of the muscle and, in the case presented in Fig. lA, the spindle firing was restored approximately 2 s after the length had been fixed. After the initial length shift (Fig. lB), in parallel to a general increase in the firing rate, the Clear-cut synchronization of discharge reappearance with the moment of transition from movement to isometric conditions was observed (marked with an arrow). It is very likely that rapid increments in muscle tension, easily seen in the transitions to fixed length, led to

steady internal deformations not only in the musck itself but in the spindle under study as well. Reappearance of the spindk firing at the moment of length fixation after shortening of the musck indicates that such deformation denotes steady stretching of the spindle receptor zone. On the other hand, the opposite effects might be supposed when length is fixed after its previous increase (phases I and II). Thus, step-like changes in tension are likely to diminish the di&ence between discharge rates at phases I and III of length fuation. At the same time, these “stop-efiects” could not compktely abolish the manifestation of the movement&pendent aftereffects. Taking into account the qualitative similarity between muscle tension reactions and the spit& tiring during kngth changes, it was also interesting to test the proprioceptor tea&ions under Patrol conditions (Fig. 2). The after-egects in musck reactions were present, in this case, as a difference in steady lengths at phases I and III. In accordance with the traditional view on spindk functions one might expect that the greater the kngth of the muscle, the higher the rate of discharge of the spindle ending. Instead, quite the opposite reaction was observedz the firing rate was higher at pbase I compared with phase III, despite the inverse relationship between steady length vahtes at these phases (Pig. 2A). When the initial musck load was increa& (the arrow in Fig. 2), at 6rst a decmase in the rate difference between phases I and III was seen (Fig. 2B) together with a defmite alteration in the time course of length changes. This decmase in the rate difTereneeseems to be connected with some diminution of the rate at phase I of the tirst application of DT in Fig. 2B. The subsequent incmmen tinload(phaseIofthesecond loading in Fig. 2B) led to a sign&ant increase in the rate (note the dashed line). It seems that the main reason for the differences in the reactions to the first (after load shin) and subsequent similar changes in load is connected with the processes analogous to the stop-effects described above for Lcontrol. Supposing

After-effects in muscle spindle activity

B

993

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Fig. 3. The reaction of the spindle secondary ending from the plantaris muscle to slow linear reciprocating changes in external load applied to the muscle and its theoretical analysis. The second record of the two identical loading cycles is shown, overall duration of the cycle equal to 21 s, backsrotmd load was 3.5 N. Upper traces represent the experimentally obtained normalized plots in coordinates: tension-firing rate (A), muscle length-firing rate (B), and tension-length (C). The normafization was made to equate the amplitudes of the corresponding parameter changes in the cycle. The subscripts + , - in the notations of the branches of the trajectories denote the direction of changes in the input variable. In lower traces the experimental dependencies are given in the form of the smoothed (by eye) curves. For full explanation of these graphs see text.

that the stop-effects are evoked by internal deformarion of the spindle receptor zone during sharp deceleration of the movement, one can expect that these effects will decrease when the velocity of the preceding movement is diminished. The observed difference in movement amplitudes may be simply explained in terms of the muscle hysteresis. 17 It is obvious that because of a smooth movement pattern under P-control conditions, the decelerations and the stop-effects were less pronounced in this case as compared with L-control. Thus, the after-effects in the firing of the spindle endings are present in a similar manner during both L- and P-control. Is this similarity connected with a definite similarity between hysteretical dependencies F(L) and F(P)? To answer this question, one may compare the general appearance of these hysteretical loops obtained during slow reciprocating movements. Through choosing the correspondent relations between amplitudes of long-lasting (15-20s in duration) cyclic changes in the muscle length (L-control) and tension (P-control), it was usually possible to achieve almost full coincidence of F(L) loops obtained in both modes of servo-control, the same was shown for F(P) loops. In the present study we restricted ourselves by considering F(L) and F(P) loops obtained only under conditions of P-control.

A typical example of the secondary ending reaction to the slow finear reciprocating changes in the external load is shown in Fig. 3. Under such conditions similar reactions were usually recorded in primary endings as well. To compare F(L) and F(P) loops the gains of F, L and P signals were chosen in order to equate the ampfitude changes of all these parameters in a full cycle, thus inscribing F(P), F(L), and L(P) loops into equal squares (Fig. 3A, B and C). It can easily be noted that the F(L) loop is broader than the F(P) one, and a difference between them is more marked in the corresponding descending branches of loops: F_ (P) and F_ (L). It is obvious that the difference between F(P) and F(L) loops is due to the non-linear dependence between arguments of these functions. In so far as we can obtain this dependence experimentally as an L(P) function, it seems possible to construct a simple procedure for the transition from F(P) to F(L) and vice versa. Considering, for simplicity, the smoothed F(P) and F(L) loops, let us superimpose the similar branches of all three loops: F + (P), F + (L) and L + (P) (muscle loading, Fig. 3D), and F_(P), F ( L ) and L_ (P) (unloading, Fig. 3E). If the dependence between muscle length and tension is finear, the normalized L(P) curve would coincide with the square diagonal, whereas F(P) and F(L) curves would

994

-2. 1.

KOSTYLKOV

and

coincide one with another. This can be seen. for example, in Fig. 3D, where at a significant part of the muscle loading the function L + (P) is going near to the square diagonal, and the functions F +(P) and F +(L) are almost equal in the same range of their arguments. The general procedure of transition for F(P) to F(L) can be considered at those values of load where the length trajectory L(P) diverged significantly from the square diagonal. Let us consider on the F +(P) curve (Fig. 3D) an arbitrary point A with coordinates [P,; F +(PA)], and define the corresponding point A* on the F +(L) curve. It is obvious that ordinates of the two points should coincide: F +(L,) = F +(P,), hence, we must only determine the abscissa of point A*, this can be done through the function L, (P): L,. = L +(PA). In a given case, when L +(P) trajectory is going below the square diagonal, L,, is placed to the left of the abscissa of the initial point A: LA. < P, (note that the comparison of the normalized values of length and tension is a correct procedure). Thus, point A* will be shifted to the left from point A and the whole trajectory F +(L) will be shifted in a similar manner, when compared to the trajectory F + (P) at this initial part of the muscle loading cycle. Using the same procedure, a transition from point B on the curve F_(P) to the corresponding point B* on the curve F (L) can be produced (Fig. 3E). The marked divergence between F I and F I curves is an expression of the pronounced hysteretical lag of the length trajectory from the tension during muscle unloading. This divergence is completely determined by the value and sign of the L (P) curve divergence from the square diagonal. The inverse transition from F(L) to F(P) is possible with the P(L) curve as the inverse function to L(P). It is obvious that full information about all the three normalized hysteretical dependencies F(P), F(L) and L(P) is contained in any pair of them. The usage of the two normalized loops F(P) and F(L) enables one to visualize the relation of the two kinds of movement-dependent after-effects (obtained with DT under P- and L-control conditions): those in the spindle ending and the hysteretical after-effects in the muscle (Fig. 3F). While neglecting the dynamic processes and stopeffects occurring under actual fixation of the muscle length or tension with DT, this procedure can be anaiysed theoretically on F(L) and F(P) loops registered during continuous slow reciprocating movements. First, let us consider the case of length fixation. Suppose that the intermediate length fixation (phases I and III of DT) is produced at the level L*, so the vertical line passing through this point (L = L*) means constant length conditions. The intersection points of the line L = L* with F(L) loop present the firing rates at phase I (C,) and at phase III (EL). The homologous points C, and E, on the F(P) loop are obtained as intersections of this loop with the two horizontal lines, passing through points

V. I.. CHEKKASSKY

C, and E,_. Note the coincidence of points C, and C,, because of the coincidence of F(L) and F(P) loops at these values of muscle length and tension. Let us denote the vector connecting points E, and C, as the isometric uncertainty vector (IMUV). The projection of this vector onto the coordinate axes give values of uncertainty in the firing rate (Y-axis) and in the muscle tension (X-axis). Both these types of uncertainty are positive and IMUV is located in the first quadrant. The ratio between the rate uncertainty and the tension uncertainty, which is determined as the slope of this vector, is also positive. Second, let us consider the case of load fixation. We take P*, coinciding with the point L* on the X-axis, as an intermediate level of load fixation. Using the procedure analogous to the one described above for L-control, we obtain initial points C, and D, on the F(P) loop, and then find the homologous points C, and D, on the F(L) loop. In this case the vector connecting points D, and C, will be further denoted as isotonic uncertainty vector (ITUV). Its projection onto the Y-axis defines the uncertainty in the firing rate while the projection onto the X-axis defines the uncertainty in the muscle length. ITUV is located in the second quadrant and has a negative slope, which is due to the negative sign of its X-projection (the length uncertainty), while the Y-projection (the rate uncertainty) is positive, as in the case of IMUV. It is interesting to consider the possible hypothetical limit cases in location of the uncertainty vectors. (I) Muscle hysteresis is absent whereas there exists hysteretical dependency of the firing rate on the muscle length and tension. Only in this case IMUV and ITUV will coincide and their slopes will be equal to 90 (2) Muscle hysteresis is well pronounced while the firing rate follows one of the mechanical parameters: (a) muscle length; (b) tension. In case (2a) zero uncertainty in the firing rate during L-control will lead to zero slope of IMUV, while during P-control ITUV will pass along the square diagonal and its slope will be 225”. In case (2b) zero uncertainty in the firing rate during P-control will give 180’ slope of ITUV, and during L-control the slope of IMUV will be 45 It can be shown that for any arbitrary sections of constant length and constant load in quite a wide range of P* and L* (approximately from 0.5 to 0.9) the uncertainty vectors will not noticeably change their slopes. When comparing IMUV and ITUV, it should also be noted that there is a significant difference in the ratio between the corresponding uncertainties which could be defined as the absolute value of tangent of the angle between the vector and the X-axis. This value is higher in IMUV versus ITUV, which becomes clear from comparison of the triangles C,E,EL and C,D,D, in Fig. 3F. While the force and the length uncertainties are approximately equal (E,E, % D,D,), the rate uncertainty is significantly higher in the case of length fixation

995

After-effects in muscle spindle activity

--

__----

-1

I 2.25mm

Fig. 4. Reaction of the spindle secondary ending from the plantaris muscle to the controlled changes in the external load applied to the muscle. The background load was 2.5 N. (A) Records of the firing rate (F), tension (P) and length (L); (B) the length-firing rate plot of the same reaction. Designations: I, II, III = phases of the load fixation; A F, A L = values of the uncertainty of the rate and length; open and closed circles denote the steady states of the firing rate and length at phases I and III correspondingly. The line connecting closed and open circles in B is the ITUV.

(C,E, > CrDr). Hence, one can suppose that the ratio the normalized uncertainties will be higher under L-control compared to P-control, i.e.

uncertainties

between

under

L-control

-AF I AP I is greater than the corresponding

value It is obvious that the above-described approach can be extrapolated to the cases of the actual fixation of the muscle length or load. The example of such an experiment on the secondary ending with DT under P-control conditions is shown in Fig. 4. To construct ITUV it is sufficient to connect the two steady-state rates of firing on the length-rate plot at phases III (closed circle) and I (open circle) of the tension fixation (Fig. 4B). In actual fixations of tension ITUV is located inside the F(L) loop obtained during slow changes in the input variable. This seems to be due to both manifestation of dynamic components in the reaction and the stop-effects. A set of the uncertainty vectors obtained for the primaries and secondaries during standard test procedure with DT under L- and P-control conditions is shown in Fig. 5. The data presented seem to be heterogeneous because of different numbers of units in the groups and the various number of every unit test, in which different initial values and fixation levels of the controlled variables were used. Nevertheless, the spread of the vector slopes within separate groups was rather low. It should be pointed out that both in the primaries (Fig. 5A) and the secondaries (Fig. 5B) the mean slopes of IMUVs (L-control) were closer to 90” than those of ITUVs (P-control). Hence, in accordance with the above theoretical considerations the ratio between the absolute values of the normalized

AF I AL I obtained under P-control conditions. The normalized uncertainties in steady states of the mechanical parameters of the muscle (I AP I,1 AL 1) may be treated as the static errors of the muscle (constant-error responses) and we can take them as basic values to evaluate a quality of the proprioceptors as the sensors tracking the muscle length and tension. With respect to these values the static errors of the spindle endings are higher under L-control conditions, thus the muscle spindle can be somewhat unexpectedly considered to be the tension sensor rather than the length sensor. DISCUSSION

Movement-dependent after-effects in the primary and secondary spindle endings were analysed in the present study using the DT method under L- and P-control conditions. Such after-effects might be observed as the difference in the steady-state firing rate for the same values of length or load, differing in the past changes prior to fixation. Movement-dependent after-effects were similar in the primary and secondary endings, being qualitatively the same for these proprioceptors under L- and P-control conditions. Both under isometric and isotonic conditions the

996

A.I. KOSTYUKOVand V. L. CHERKASSKY

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F

1.0 0

Fig. 5. IMUVs and ITUVs obtained for the reactions of the spindle endings to the controlled changes in the muscle length (L-control) or the external load (P-control) with using the double trapezium as a command signal to the stretcher (results of many experiments). (A) Primary spindle endings (m. gastrocnemius); (B) secondary spindle endings (In. plantaris). NormaliTation of the data was made using the following formulae: I~ = ( F - F o ) / ( F I I

- Fo);

f'- = ( L - L o ) / ( L I I

- Lo),

P = (P - Po)/(Pt!

- eo),

where the corresponding parameters with subscripts O and II denote their steady-state values before double trapezium and at phase II. Closed and open symbols denote the beginning (phase Ill) and the end (phase I) of the uncertainty vectors. Various symbols (circles, squares and triangles) belong to the different units from the same totafity, N -- number of units, n = total number of tests. The mean values and their 95% confidence intervals were computed using two-tailed t-test for the slopes of the uncertainty vectors within every totality (~,); these parameters are also shown 8raphically as arrows and filled segments in the circle diagrams. The range of relative values of the level of the controlled variable fixation (the amplitude of the variable at phases I and III with ~ to the amplitude at phase II) was 0.44--0.67 (A); 0.55-0.76 (B) for L-control and 0.5--0.69 (A); 0.48-0.8 (B) for P-control. Maximal stretchin~ of the muscles at phase III in L-control in various experiments ranged from 8 to 14 ram, maximal loads at phase III in P-control were in the range of 6-12N.

steady rates of spindle ending discharges were invariably higher after previous muscle lengthening (loading) versus shortening (unloading). The difference between these rates, i.e. the uncertainty in steadystate firing, could be as large as 15-20 p.p.s. The movement-dependent after-effects in reactions of spindle endings might be somewhat decreased by an oppositely directed action of the so-called stopeffects. The latter are probably connected with the sharp deceleration in the muscle movement, hence it is obvious that these processes should be most pronounced under L-control conditions because of, as a rule, the significantly lower values of deceleration under P-control. The hypothesis about mechanical origin of the after-effects evoked in the primary endings of muscle spindles by preceding fusimotor stimulation has been stated in the works by Hunt e t al. ~6 and Kuflier e t al. 20 This hypothesis has been further developed. 3,s-7,H'3° Based on the conceptions about the muscle contrac-

tion mechanisms, first formulated by Hill, ~ Brown supposed that the conditioning fusimotor stimulation evoked the formation of stable crossbridges between actin and myosin myofilaments in the intrafusal muscle fibres. These stable transverse bounds lead to a significant increase in the stiffness of the intrafusal fibres belonging to a given spindle, thus increasing the deformation of its receptor zone during the testing procedure: standard muscle lengthening and/or fusimotor stimulation. One of the main arguments supporting the mechanical origin of the fusimotor after-effects is the fact that they are easily destroyed by muscle lengthening of 4-5 mm. At the same time, some contradictions arose, when the processes of after-effects destruction were studied in detail. In this context, the study of Proske 29with the series of triangular muscle lengthenings used as a test of the fusimotor after-effects must be mentioned. A paradoxical facilitation was observed in primary ending e t al. 3

Afkweffects in muscle spindle activity responses to test stimulation of the dynamic y-axon, provided that the triangular changes in length were large enough. On the other hand, Morgan et al+?’ who used almost the same cyclic len~h~~, showed a significant decmase of the primary ending responses to the test y,-stimulation. Moreover, if the muscle was fixed at the apex of the last cycle and was then shortened to the initial length, the responses to the test decreased significantly compared with the standard cyclic kngth changes. Using the asymmetrical triangular muscle lengthening with the more rapid reverse phase as compared with the forward one, Emonet-D&and et a1.6showed that such movements without any fusimotor stimulation could evoke aftereffects in the primary ending firing which were similar to the fiisimotor ones. Thus, it is supposed that the after-effects might be connected not only with the preceding firsimotor activation of the spindle but also with the definite, pure mechanical manoeuvres of the muscle. We also suppose that some steady changes in the mechankal state of the spindle intrafusal fibres underlie the after-effbcts in the firing of the spindle endings. These changes are a result of the residuaf effects of the hysteresis (thixotropy) in intrafusal muscle fibres. The hysteretical after-effects in the tetanically activated mammahan muscle are present, in particular, as two, essentially different steady-state lengths at equal loads, provided that these parameters changed in opposite directions before fixation.” By varying both the load and the rate of efferent stimulation, it has been shown that two steady lengths exist in this case as well, and which of these two was ilnally set up for given tied kvels of the two input variables, depended only on the direction of the previous movement, but not on the actual time course of these variables.‘* Considering these results, one can easily understand the action of the conditioning fusimotor stimulation under isometric conditions. Active shortening of the intrafusal fibres is followed by their passive lengthening after the stimulation has been switched off. Thus, the kngthening of the intrafusal fibres constitutes a functionally significant movement in this case. It increases the stiffness of the spindle and, hence, its responsiveness to the subsequent test disturbances. But just the same effect can be achieved through the cyclic shortening movement of muscle, which produces lengthening of the intrafusal flbres at its last phase. Thus, both the fusimotor and the movement-dependent after-effects seem to allow their unified treatment on the basis of hysteresis in intrafusal muscle fibres. It is noteworthy that the reciprocating cycle of muscle lending usually used to test the aftereffects is generally referred to as “lengthening”. In fact, this is a complex movement composed of two phases. Aftereffects of the muscle hysteresis are completely determined by the direction of movement before its cessation, the shortening in a given case. Hence, this movement can be considered as leading

997

not to the destruction of the preceding fusimotor after-effects, but rather to the formation of the movement-dependent after-effrcts connected with the shortening of the intrafusal fibres. It becomes clear why only large amplitudes (44mm) of the cyclic lengthening are needed to destroy the fusimotor after-effects.s Small movements cannot produce any significant hysteretical after-effects in the intrafusal fibres. The a~v~rn~tio~ activation of muscle spindles during asymmetric trkng&r movements in the study of Emonet-D&and et uJ.~ seems to be a result of the stop-effects, which should be increased with the rise in velocity of the last movement phase. As regards the paradoxical observation of Proskea for the spindle activation by quite slow cyclic kn~~n~, it seems to be a result of the specific time course of length changes used in this study. An undershoot can be seen at the latest phase of these changes before length fixation, i.e. the muscle was lengthened at the final part of movement (see Fig. 1 from Proskfl. In the present study we made an attempt to de6ne the relations between the mov~ent~~dent after-effects and hysteresis of the spindle firing. Lennerstrand” and Lennerstrand and Thodenzfz5 produced a comprehensive quantitative analysis of the spindle ending activity during cyclic changes in muscle length. A ckar-cut loop-shaped form of the kngth-gring rate plots for very slow change in the muscle length enabled them to make a conclusion about powerful hysteretical components in these reactions. We studied the hysteretical effects in the spindle firing because these effects were very likely to underlie the formation of the movement-dependent after-effects. To analyse the relationship between the hysteretical properties of the proprioceptor ih-ing and the after-effects, it was necessary to study, in addition to the length-rate dependence, the tension-rate as well. Moreover, comprehensive analysis of the spindle hysteresis proved to be impossible without taking into account the hysteresis inherent to the muscle. The analysis of the relation between hysteretical effects of the spindle with those of the muscle was performed by comparing the cyclic F(P) and F(L) dependencies normalized by the amplitude changes of the corresponding variables in the cyck. The two sets of uncertainty vectors were introduced: ITUVs, connecting the points with the equal load on the F(L) loops, and IMUVs, connecting the points with equal length on the F(P) loops. The projections of both uncertainty vectors onto the Y-axis gave the firing rate uncertainties, being positive, whereas their projections onto the X-axis differed in sign being positive for IMUV (the tension uncertainty~ and negative for the ITUV (the length uncertainty). Because of such a combination in signs of the unartainty vector projections, the ITUVs were always located in the second quadrant and the IMUVs in the first one. The closer the vector slope to 9Q”, the more pronounced is the ma~f~~tion of the hysteretical effects in the propri-

998

A. 1. KOSTYUK~V and V. 1.

oceptor activity proper, compared to the muscle hysteresis. Statistical analysis of the data obtained with DT method under P- and L-control conditions showed that in both primary and secondary endings IMUVs were closer to 90” compared to the ITUVs. The averaged angles were 60.3 + 3.3” (primaries) and 70.0 + 3.9” (secondaries) for IMUVs, and 131.O + 4.2” (primaries) and 130.0 & 4.6” (secondaries) for ITUVs. Thus, the relation between the static errors in the spindle firing and the hysteretical uncertainties in the muscle mechanics is higher for the length tracking by these propcioceptors as compared to the load tracking. The conclusion that the spindle firing rather follows the tension changes than the length ones has been made from the experiments on de-efferented muscles, but it may also probably be extrapolated to the case of intrafusal activation of the spindles. The close proximity between spindle ending activity and muscle force has been shown in human experiments by Vallbo, 36 but in this study the analysis was restricted by isometric conditions. Additionally, continuous fusimotor stimulation of the spindle does not abolish the movement-dependent after-effects, which can be observed, for example, in the records presented in the studies of Boyd et al2 and EmonetDenand et aL5 For slow reciprocating changes in the muscle length the hysteretical form of the lengthfiring rate dependencies was also not changed by fusimotor stimulation although sometimes the loops became narrower.24 At the level of spinal reflexes the hysteretical effects in the activity of spindle endings seem to enhance the hysteresis of the muscle itseff. In decerebrate animals the stretch-reflex being tested with cyclic changes in the muscle length showed a pronounced hysteretical

CHEKKASSKV

dependence of tension on length.26.-12On the other hand, as compared with the reactions of de-efferented muscle, the muscle hysteretical after-effects, such as un~~inty in equilib~um length, were also shown to be enhanced by the stretch-reflex.” It seems that the usage of simplified linear models, such as the spring model of the muscle and the visco-elastic model of the muscle spindle, should be somewhat restricted for the analysis of motor pcrformance. Based on these models, the so-called equilibrium point hypothesis has been formulated.9,i0 It is obvious that this hypothesis leads to the conclusion about unambiguity of equilibrium state in the system joint-load. At the same time, it is well known that previous muscle activation as well as some movement manoeuvres can largely modify various spinal reflexes.8,‘2,u,33 One of the reasons for this modification seems to be due to the hysteretical effects in the spindle activity.

CONCLUSION

The present study was restricted by the analysis of firing in the spindles deprived of fusimotor inflow; the parent muscle was also passive. Regardless, the results obtained do not pretend to explain actual situations with the variety of possible patterns of extra- and intrafusal activation and muscle movements. However, we hope that they will contribute to the development of some experimental approaches to solve these problems. Acknowledgements-The technical assistance of N. Zaitseva and V. Ivanenko, and technical support by V. Komeev are greatly appreciated. Thanks to Dr A. Tal’nov for valuable discussion of the manuscript.

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