430 J. Phy8iol. (1965), 179, pp. 430-441With 6 text-figuresPrinted in Great Britain

MUSCLE STRETCH AND THE PRESYNAPTIC INHIBITIONOF THE GROUP Ia PATHWAY TO MOTONEURONES

BY M. S. DEVANANDAN, ROSAMOND M. ECCLESAND T. YOKOTA*

From the Department of Physiology,Australian National University, Canberra, Australia

(Received 16 November 1964)

It has been shown that the monosynaptic EPSP which was evoked ina motoneurone by a volley in its muscle nerve could be depressed byconditioning volleys in other muscle nerves without any evidence of post-synaptic inhibitory changes in the motoneurone (Frank & Fuortes, 1957;Eccles, Eccles & Magni, 1960, 1961). Eccles et al. (1961) described the timecourse of this EPSP depression and related the depression to volleys innerves from muscles with different functions. In general, activity innerves from flexors evoked greater depression of the monosynaptic EPSPthan volleys in nerves from extensors. It seemed that a correlation existedbetween the EPSP depression and the dorsal root reflex (DRR) and thatboth these phenomena are due to the same process, viz. depolarization ofthe primary afferent fibres within the spinal cord. Eccles, Magni & Willis(1962) provided conclusive evidence of the depolarization of centralterminals of group I primary afferents from muscle. This depolarizationfollowed the same time course as the EPSP depression and is evoked underthe same experimental conditions. This phenomenon was designated'presynaptic inhibition'.Devanandan, Eccles & Yokota (1965) observed that depolarization of

the central terminals of primary afferent fibres can be produced by musclestretch. It will be shown in this paper that muscle stretch may effectivelydepress the monosynaptic EPSP and the monosynaptic reflex. Thisdepression of the monosynaptic reflex was strychnine resistant, therebyestablishing that it was not due to post-synaptic inhibition (Bradley,Easton & Eccles, 1953).

METHODS

The experimental techniques have been described in full in the earlier paper (Devanandanet al. 1965) as well as in other publications (Eccles, Kostyuk & Schmidt, 1962; Eccles,Schmidt & Willis, 1963).

* Rockefeller Fellow.

DEPRESSION OF GROUP Ia PATHWA YTo record monosynaptic reflexes, the ventral roots L 6-S 1 were cut and the central ends

of the L 7 and S 1 ventral roots were prepared for recording. For studies on the monosynapticEPSPs the ventral roots were often left intact so that the motoneurone impaled could beaccurately identified by antidromic invasion (Eccles, Eccles & Lundberg, 1957a).

Presynaptic inhibition was demonstrated by the depression of the monosynaptic excita-tory post-synaptic potential (EPSP), the membrane potential remaining constant, and bythe depression of the monosynaptic reflex. When recording reflexes selective depression ofpost-synaptic inhibition was effected by strychnine in an initial intravenous dose of 0-08 mg/kg, and this dosage was later increased in order to show that the inhibition was trulystrychnine resistant. Generally strychnine could not be given during intracellular recordingbecause strychnine convulsions often dislodged the micro-electrode from the motoneurone.However, six motoneurones were examined after intravenous strychnine (0-1 mg/kg) andone of these motoneurones is illustrated in Fig. 6.

RESULTS

Depression of the monosynaptic EPSPThe presynaptic inhibitory pathways have been shown to depolarize the

primary afferent fibres (Eccles et al. 1961; Eccles, Magni & Willis, 1962),thereby causing a reduction of transmitter release from the primaryafferent fibres (Takeuchi & Takeuchi, 1962; Eccles, 1964). This leads toa reduction in size of the monosynaptic EPSP of a motoneurone withoutan alteration in its membrane potential (Frank & Fuortes, 1957; Eccleset al. 1961).

In Fig. 1 the monosynaptic EPSP evoked by a volley in the plantarnerve was preceded by a stretch of the DP muscles at the indicated inter-vals, the recording conditions being given by Fig. 1 of the preceding paper(Devanandan et al. 1965). The EPSP was depressed to about 83% of thecontrol height in 30 msec. The depression had a total duration of about130 msec. From the inset it can be seen that stretch of the DP muscleevoked only a small brief EPSP in the motoneurone under observation.

In Fig. 2 a volley of group I strength in the GS nerve evoked an EPSPin a gastrocnemius motoneurone that was conditioned by a stretch appliedto the PDP muscles. The presynaptic inhibition was greater, the EPSPbeing depressed to 70% of the control height, but both the maximumdepression at 30 msec and duration of 140 msec were similar to thoseobserved in flexor motoneurones (Fig. 1). Stretch of the PDP musclesproduced a post-synaptic inhibitory potential (IPSP) of short duration(see inset).

Finally, in Fig. 3 the effects of conditioning with applied stretches toeither ST or PDP are recorded. The monosynaptic EPSP in the plantarismotoneurone was small but constant. The peaks of the EPSP depressionsin response to stretches of ST at 40 msec and of PDP at 35 msec wereslightly later than those recorded in Figs. 2 and 3. The durations were long,though not observed as a smooth recovery over 120-140 msec. The earlier

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M. S. DEVANANDAN AND OTHERS

depression evoked by a PDP stretch (Fig. 3D) was probably due to thepost-synaptic inhibitory action byPDP group I a fibres on to motoneuronesof the antagonistic group, i.e. ankle flexors on to ankle extensors.

It seemed that conditioning with applied stretch of the PDP muscle wasnot as effective in producing EPSP depression as a tetanus applied to thecut PDP nerve (Eccles et al. 1961). It was found that, if electrodes wereplaced around the intact PDP nerve, application of stimuli to theseelectrodes always evoked much larger EPSP depressions than musclestretch.

A limVCON 2fK 36/N 60 87 104

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Fig. 1. In the graph (B) are the plotted heights of the monosynaptic EPSPs in aplantar motoneurone evoked by a volley in the plantar nerve, and preceded byactivation of the muscle receptors ofDP muscles. Samples of the records are givenabove (A) with numbers indicating the time between conditioning and testingstimuli in msec. Potential and time scales the same for all records. The 100% ofthe graph is the size of the control EPSP. Duration of stretch of DP muscle was10 msec as shown. Inset is a record of the effect of the muscle stretch on the mem-brane potential of the impaled motoneurone. The arrow marks the end of the pullartifact. The EPSP produced by the stimulation of the plantar nerve is seen as thelarge deflexion at the end of the record, the upstroke having disappeared. Thevoltage calibration is the same as in A. Pull used about 160 g.

Reflex testing

In a monosynaptic reflex the number of discharging motoneurones isapproximately proportional to the size of the spike potential in theappropriate ventral root. The monosynaptic reflex is set up by stimulationof the muscle nerve in the periphery. The largest afferent fibres (I a) in themuscle nerve synapse directly on to the motoneurones. If the excitation isabove a threshold level, a spike is initiated and propagates down theaxon. Any alteration in the excitability of the afferent fibres, or their

432

DEPRESSION OF GROUP Ia PATHWA Y

terminals, or the motoneurones will be signalled by a change in the reflexsize. Consequently a monosynaptic reflex is a valuable guide to excit-ability changes in the largest afferent fibres from muscle (Ia).

In Fig. 4 the testing situation was the facilitated monosynaptic reflexfrom stimulating posterior biceps nerve (PB). Since the unfacilitated PBreflex was rather unstable, it was facilitated by an earlier conditioningvolley in the PB nerve which alone did not evoke a reflex. A stretch wasapplied to the DP muscles at various intervals preceding the facilitatedPB reflex. The depression evoked is shown by the graph (open circles,

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Fig. 2. The monosynaptic EPSPs evoked in a gastrocnemius motoneurone by avolley in gastrocnemius nerve were conditioned by stretches applied to the PDPmuscle at the times indicated on the graph B. The 100% level was the size of thecontrol EPSP. Duration of the stretch was lO msec. Some ofthe EPSPs from whichthe graph was constructed are shown above with their potential and time scales.Inset is a record of the effect of the muscle stretch on the membrane potentials ofthe GS motoneurone. As the record shows, a transient hyperpolarization is evokedby the muscle stretch. The voltage calibration is the same as in A. Pul] used about395 g.

Fig. 4). Typical responses from which this graph was derived are givenin Fig. 4A. The depression reached a maximum at about 50 msec andrecovered first quickly and from 90 msec onwards more slowly. It isrealized that activity of the afferent fibres either by stretching the stretchreceptors or stimulating the nerve (Eccles et al. 1963) may evoke bothpost-synaptic effects and presynaptic effects in the spinal cord. Forexample, impulses in lb fibres of a flexor muscle can depress the excit-ability of the PB Ia afferent fibres (i.e. presynaptic inhibition). Also,impulses in Ib fibres from a muscle flexor can evoke post-synaptic excita-tion of PB motoneurones (i.e. post-synaptic excitation up to 40 msec in

28 Physiol. 179

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M. S. DEVANANDAN AND OTHERS

ACOJ6'[1 mV

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MillisecondsFig. 3. The intracellular monosynaptic EPSPs from a plantaris motoneuroneevoked by a volley in plantaris nerve were conditioned at different intervals byapplied stretches to the ST muscles (A and B) or the PDP muscles (C and D). InB and D the full time course of the effectiveness of stretches applied to ST muscle(B) and PDP muscle (D) are plotted. Duration of stretch again was 10 msec. InA and C are the examples of some of the EPSPs recorded. Note that A and Chave their own potential and time scales. The insets show the effect ofmuscle stretchon the membrane potential of the impaled cell, the voltage calibration in each casebeing the same as that given above the respective graph. Pull of ST muscle about177 g. Pull of PDP muscles about 450 g.

434

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DEPRESSION OF GROUP Ia PATHWA Y

graph of Fig. 4) though some inhibitory effects may be seen (Eccles, Eccles& Lundberg, 1957 b). One can distinguish between these inhibitions in twoways: the post-synaptic inhibitions are generally shorter than presynapticinhibitions (Eccles, Schmidt & Willis, 1962) and strychnine blocks post-synaptic inhibitions and usually increases presynaptic inhibitions (Eccleset at. 1963). Since the depression of the facilitated PB reflex (Fig. 4, opencircles) showed a second component at 80 msec, strychnine (0- 1 mg/kg) wasadministered intravenously. This increased the inhibition and also greatlylengthened the time course (Eccles et al. 1963). It will be noted thatstrychnine increased the earlier phase of excitation (cf. the records in

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Fig. 4. The monosynaptic reflex evoked by PBST was recorded in the central endof S1VR (CON in A) and conditioned by a pull (10 msec in duration) applied to theDP muscles (row A and open circles). Row B and filled circles on graph were

recorded after a dose of strychnine, 0-1 mg/kg. Open circles on graph, beforestrychnine. Same potential and time scales for A and B. Pull about 160 g.

Fig. 4A and B at 28 msec). This is a typical result of strychnine admin-istration and probably indicates an increased excitability of the moto-neuronal membrane due to an increased background of interneuronalactivity. Often the sizes of the monosynaptic reflexes were increasedafter strychnine. If this occurred the control reflex was kept approxi-mately to the same size as that before strychnine administration (i.e. thecontrol reflex of the B series would equal the control reflex of the A series).

28.2

435

120

100

436 M. S. DEVANANDAN AND OTHERS

Since, in this particular experiment, the control reflexes were approxi-mately equal and no adjustment of reflex size was required, it was probablethat the majority of motoneurones were firing even before the drug wasgiven.

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Fig. B. The monosynaptic reflex evoked by stimulation of the nerve from the GSmuscle was recorded in the central end of SlVR. In A and filled rectangles in Cthe effect of conditioning with ST muscle stretch (10 msec duration) was investi-gated to weak pulls (2-5 V about 46 g) and to stronger pulls about 177 g (B andopen rectangles (C)). The effect of increasing strength of the muscle stretch(abscissa) is plotted (in D) against the depression recorded (ordinate).

In Fig. 5 after a conditioning stretch of the ST muscle the facilitatedreflex to stimulation of the GS nerve was recorded in the S1VR. When asmall pull (2 5V) was applied to the ST muscle the inhibition was less than

DEPRESSION OF GROUP Ia PATHWAY

20% (Fig. 5C or the record taken at 29 msec in Fig. 5A). The time coursefor the inhibition was 100 msec. If the strength of pull was altered to10V there was a much larger depression (open squares, Fig. 5C), withalmost complete inhibition of the GS reflex at 25 msec and later at 60-70 msec. The early depression could definitely be post-synaptic inhibitionsince no strychnine was given to this animal, but the long, late, seconddepression seems to have a time course similar to those described alreadyfor presynaptic inhibition. Even at 140 msec the reflex is depressed bymore than 40 %. At a fixed interval in Fig. 5D when the strength of pullwas altered there was a sharp distinction between 3 and 5V. This wasquite repeatable so that one can assume that a voltage of 2 5V stimulatesonly the most sensitive receptors whilst for all stretches evoked by 5V ormore a maximum effect is obtained.These changes on the monosynaptic reflex could be due either to a

motoneuronal change or to an alteration in the excitability of the afferentfibres. It seemed likely to be presynaptic in origin since the excitabilitychanges (Devanandan et al. 1965) were not unlike those associated withpresynaptic inhibition, particularly regarding the long durations observed,and strychnine was ineffective in reducing the inhibitions observed (Eccles,Schmidt & Willis, 1962, 1963).

Finally, in Fig. 6, the relation between EPSP depression and reflexdepression is illustrated when all post-synaptic inhibition would have beeneliminated by strychnine (Bradley et al. 1953). The monosynaptic EPSPfrom an impaled GS motoneurone was displayed on one beam of theoscilloscope, and the unfacilitated monosynaptic GS reflex recorded in theS, ventral root was recorded on the other. A 1OV pulse was employed toelicit stretches of the PDP muscles. The EPSP was depressed to about80% of the control, whereas the reflex was depressed much more (about40% of the control). This illustrates that, though the depression of theindividual EPSPs may not appear to be large when conditioned with amuscle pull, the excitability of the whole motoneurone pool may be con-siderably depressed.

DISCUSSION

The motoneurone pool is subject to several influences that converge onto it from the periphery, from within the spinal cord and from supra-spinalregions. The net result of these several factors will tend to activate ordepress a given motoneurone pool. Since the index of activity has beenthe monosynaptic reflex or monosynaptic EPSP, only the group I aafferent fibres in the stimulated peripheral nerve will be responsible for thisactivity (Lloyd, 1943). This reflex or EPSP has been preceded by a musclestretch at various intervals, and the resulting depression of the reflex or

437

438 M. S. DEVANANDAN AND OTHERS

EPSP noted. The control monosynaptic reflexes and EPSPs taken atfrequent intervals during the experiments were very stable. Therefore, thedepression noted, when the conditioning muscle stretch was applied, was

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Fig. 6. The monosynaptic EPSP of a GS motoneurone was recorded on one beamof the oscilloscope, upper row of records. Simultaneously the unfacilitated GSmonosynaptic reflex was recorded in S1VR and displayed on the other beam,lower row of records. The effect of stretching the PDP muscles with a pull of about450 g is plotted on the graph. The filled circles follow the time course of the EPSPdepression; the open circles the time course of the reflex depression. Inset is theeffect of the muscle stretch on the membrane potential of another GS motoneuroneclose by, as the motoneurone used for the records illustrated in the graph was lostbefore the effect of muscle stretch on the membrane potential could be recorded.Note strychnine (0-1 mg/kg) was administered intravenously before this moto-neurone was impaled.

due to a change in the synaptic events involved rather than to anyspontaneous variation in the excitability of the motoneurones.

In the present series of experiments, monosynaptic EPSPs in GS, PL orplantar motoneurones have been conditioned by stretches of the flexor

DEPRESSION OF CROUP Ia PATHWA Y

muscles, ST, DP or PDP. Care was always taken to check whether themuscle pull produced an IPSP in motoneurones in each case (see insets inFigs. 1, 2 and 3). In agreement with Eccles & Lundberg (1959) it can beseen that the effect of muscle stretch on the plantar motoneurone wasexcitatory, and the stretch of the ST muscle had no effect on the PLmotoneurone. On the other hand, the stretch of the PDP muscles didevoke IPSPs in the PL and GS motoneurones. However, the depression ofthe monosynaptic EPSP is unlikely to have been greatly affected as theEPSP remained depressed long after the IPSP had disappeared. Also ithas been shown that direct inhibition will reduce the size of the EPSPonly if the EPSP falls within 2 msec of the start of the IPSP (Coombs,Eccles & Fatt, 1955).When the testing situation was the monosynaptic reflex, post-synaptic

inhibition was generally discounted by the use of strychnine (Bradleyet at. 1953). Also, the group I afferents from the ST have little or no post-synaptic effects on the motoneurones of the physiological extensors of theankle (Eccles & Lundberg, 1959), and the post-synaptic actions of the DPmuscle afferents are, if anything, excitatory on the PB motoneurones(Eccles & Lundberg, 1959). Therefore, the EPSP depression and reflexdepression reported here are probably due to presynaptic inhibition.

It has been shown (Fig. 5C and D) that increasing the intensity of thepull to a certain level increases the amount of inhibition. This has beenobserved constantly. When the responses from the muscle stretch re-ceptors were analysed by recording from filaments in the dorsal root, it wasalways noticed that the increase in inhibition coincided with the activationof the Ib afferents (Fig. 6; and Devanandan et al. 1965). This is in agree-ment with previous results from electrical stimulation of muscle afferentfibres (Eccles, Schmidt & Willis, 1962).The differences in the experiments reported above and those in a com-

munication from Granit, Kellerth & Williams (1964) may be in the tech-niques employed. Granit et al. (1964) stated that no presynaptic inhibitionwas observed when the behaviour of motoneurones was directly observedduring applied stretches to muscle. These authors employed only largestretches with slow rates of rise and maintained for several seconds. Incontrast, only rapid brief stretches (10 msec in duration) have beenemployed here. In our experiments we have been only concerned withthe period subsequent to the muscle stretch so that the long-lastingdepressions would be recorded, after 40 msec or so, uncontaminated bypost-synaptic events on the motoneurones themselves. These long-lastingdepressions of both the monosynaptic EPSPs and reflexes have been shownto be presynaptic inhibitory effects since they persist after strychnineadministration.

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M. S. DEVANANDAN AND OTHERS

Since it has been shown that muscle stretch can evoke presynaptic in-hibition, it becomes necessary to study it in greater detail taking into con-sideration the patterns of activation of the muscle stretch receptors andtheir reflex regulation through the y-motoneurones. The response of theprimary spindles to stretch can be divided into a dynamic response and astatic response (Jansen & Matthews, 1961; Matthews, 1964). Renkin &Vallbo (1964) have suggested that they register the instantaneous velocityof stretch and the instantaneous length of the muscle. The presynapticinhibition evoked by the Ia afferents must therefore be analysed in regardto these two different responses, both with y-loops intact or interrupted.Jansen & Rudjord (1964) suggested that the Golgi tendon organs are con-traction receptors rather than stretch receptors. The presynaptic inhibi-tion evoked by the lb afferents should therefore be examined duringmuscle contraction as well as muscle stretch.

SUMMARY

1. The monosynaptic EPSPs of motoneurones of extensor muscles ofthe ankle, and of a flexor muscle of the foot were conditioned by stretchesof flexor muscles of the knee or the ankle.

2. The EPSPs were depressed by the muscle stretches over a timecourse of about 120-140 msec, the peak being at about 30 msec.

3. The monosynaptic reflexes of extensor muscles of the ankle andflexor muscles of the knee were similarly reduced by conditioning withapplied stretches of flexor muscles of the ankle or the knee.

4. This depression of the reflex and the EPSP could not be abolished bystrychnine and therefore was not due to post-synaptic inhibition.

5. It is suggested that these depressions are due to presynaptic in-hibition.

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COOMBS, J. S., ECCLES, J. C. & FATT, P. (1955). The inhibitory suppression of reflex dis-charges from motoneurones. J. Physiol. 130, 396-413.

DEVANANDAN, M. S., ECCLES, R. M. & YOKOTA, T. (1965). Depolarization of afferentterminals evoked by muscle stretch. J. Physiol. 179, 417-429.

ECCLES, J. C. (1964). The Physiology of Synapses. Berlin, G6ttingen, Heidelberg: Springer.Verlag.

EccLEs, J. C., ECCLES, R. M. & LUNDBERG, A. (1957a). The convergence of monosynapticexcitatory afferents on to many different species of alpha motoneurones. J. Physiol. 137,22-50.

ECCLES, J. C., ECCLES, R. M. & LUNDBERG, A. (1957b). Svnaptic actions on motoneuronescaused by impulses in Golgi tendon organ afferents. J. Physiol. 138, 227-252.

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DEPRESSION OF GROUP la PATHWAY 441ECCLES, J. C., ECCLES, R. M. & MAGNI, F. (1961). Central inhibitory action attributable to

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