Reciprocal Inhibition Contract Muscle

8/2/2019 Reciprocal Inhibition Contract Muscle

1/9

Exp Brain Res (1984) 53:400-408

(9 Springer-Verlag 1984

Changes in Rec iproca l Ia Inh ib i t ion During Voluntary Contract ion in ManM. Shindo 1, H. tt arayama 1'3, K. Kondo t, N. Yanagisawa 1, and R. Tanaka 21 Dept. of Medicine (Neurology), Shinshu University School of Medicine, Asahi 3-1-1, Matsumoto, Japan2 Dept. of Neurobiology, Tokyo Metropolitan Institute for Neurosciences, 2-6 Musashidai, Fuchu City, Tokyo, Japan

S u m m a r y . Reciprocal Ia inhibition from ankle flex-ors to extensors was studied during voluntary tonicisometric dorsiflexion and plantar flexion in fivenormal subjects. The Ia inhibition was examined asthe short-latency suppression of the soleus H-reflexesby stimulation of the low-threshold afferents in thecommon peroneal nerve (Mizuno et al. 1971). Atrest, weak la inhibition was demonstrated in foursubjects out of five, the maximal amount being 14.1+ 5.0% suppression of the control H-reflex. Theabsolute amount of inhibition, which was calculatedby subtracting the mean size of the conditioned H-reflex from that of the control H-reflex and expressedas a percentage of the maximal M-response, in-creased during ankle dorsiflexion, and decreased ordisappeared during plantar flexion in parallel withthe amount of contraction. The neural mechanismsfor facilitation of the Ia inhibitory pathway duringdorsiflexion were considered to support thehypothesis of "a-y-linkage in reciprocal inhibition",i.e. combined facilitatory effects on the Ia inhibitoryinterneurone from the supraspinal centers directlyand indirectly via the y motoneur one - Ia afferentroute. The mechanism for inhibition of the pathwayduring plantar flexion was considered to be inhibitionof the Ia interneurone of the flexor side by Iainterneurone of antagonist extensors. A quantitativeaspect of activity in the reciprocal Ia inhibitorypathway on the performance of voluntary movementis revealed in this study.Key words: H-reflex - Ia irrhibition - Tonic voluntarycontraction - Ankle muscles - Man

3 Present address: Dept. of Neurology, Brain Research Institute,Niigata University, Asahimachi 1, Niigata City, JapanO f f p r i n t req u es t s t o : Dr. M. Shindo (address see above)

Introduc t ion

Reciprocal Ia inhibition is considered to be one of themost important neural mechanisms in the perfor-mance of movements, and it has been extensivelyinvestigated in animals (Eccles 1969; Lundberg 1970;Hultborn 1972; Baldissera et al. 1981). It has beenestablished that the interneurone mediating disyn-aptic Ia inhibition is under the control of varioussupraspinal and segmental systems, and it has beensuggested that this interneurone plays the role of anintegrative center in reciprocal innervation.

In man, the Ia inhibition was revealed initially insubjects with certain neurological disorders (Mizunoet al. 1971; see also Yanagisawa et al. 1976;Yanagisawa and Tanaka 1978; Yanagisawa 1980). Itappeared as a very short latency inhibition of the H-reflex in the ankle extensors following stimulation ofthe low-threshold afferents in the antagonistperoneal nerve. Ia inhibition of ankle flexors by tibialnerve stimulation was also demonstrated. Ia inhibi-tion from the ankle flexors to the extensors has beenobserved in only a small fraction of normal subjectsat rest, and has always been very weak (Tanaka 1974,1980). Tanaka, however, demonstrated it to appearconstantly during voluntary dorsiflexion of the foot.The threshold for this inhibition was lower instronger contraction than in weaker contraction. Onthe basis of these observations he postulated apositive relationship between the excitability of theIa inhibitory pathway and the amount of contraction.In order to investigate this more precisely we studiedthe quantitative relationship between amounts of Iainhibition and voluntary contraction; Ia inhibition onthe ankle extensors from the flexors was studied atrest and during several strength stages of tonicvoluntary dorsiflexion and plantar flexion of the foot.


2/9

M. Shindo et al.: Changes in Reciproc al Ia Inhibition During Voluntar y Contra ction in Man 401oSCillOSCOpe~--------------~arotine

~ J ~ l - w a v e r e c ti t~ l~ O r ~ [~_gated integrator!~ - ~ ] recticorder

9 data recorderFig. 1. Schematic illustration of experimental setting

M e t h o d s

The study was made on five healthy male volun teers (ages between26 and 33). Most subjects were examined 2-4 times on differentdates. The subject was comfortably seated in a reclining armchair.The leg was fixed to an immobile foot-plate which was connectedto a torque meter. The thigh was fixed to the chair and the foot tothe foot-plate with leather bands. The angles of the knee and anklejoints were kept at about 120 and 100 deg, respectively.

The experimental setting is shown in Fig. 1. Electromyogramwas recorded bipolarly with surface electrodes. Th e paired elec-trodes were pla ced 3--4 cm apar t longitud inally over the soleus,just below the gastrocnemiu s muscle belly, and the tibialis anter iormuscles. The EMGs were amplified with conventional amplifiers(T.C. = 0.05 s, high cut = 1 kHz), and were record ed on an ink-writing recticorder (Nihon Kohden, WI-640G) and on a datarecorder (Sony, DFR-3515).

Conditioning stimuli were applied monopolarly to the com-mon peroneal nerve at the level of the caput fibulae. A needle orsurface electrode was used as cathode, and a surface plateelectrode was placed anterior to the caput fibulae as anode. Thestimulating pulse had a duration of 1 ms, and the strength was0.9-1.2 times the threshold for the M-response (XMT) in thetibialis anterio r muscle. Single or 2-3 pulses with intervals of 3.5ms were delivered. The position of the cathode electrode wasadjusted in order to evoke contraction of the tibialis anteriormuscle, but not the peroneal muscles, at the lowest motorthreshold. For evoking test H-reflexes in the soleus muscle thetibial nerve was stimulated in the popliteal fossa with surfaceelectrodes. The stimulus was a single pulse of 1 ms duration, thestrength being adjusted to obtain the maximal H-reflex and also H-reflexes with amplitudes between % and % of the maximum. Asmall M-response was obtained with the maximal H-reflex. Thestability o f the stimulating condit ions was monitor ed by this smallM-response throughout the experiment.It was essential to ensure that stimu lation of one nerv e did notspread to its antagonist, and for this purpose the electrode settingswere adjusted so that the conditioning stimuli to the flexor nervenever evoked M- or H-response in the extensor muscles even witha strength of three times the threshold for the flexor M-response,and, similarly, the test stimuli to the ex tenso r nerve did not excitethe flexor muscles even when applied at a strengt h of 1.5 times thatneeded to evoke the maximum H-response in the extensors.

Recording was done at rest, and during tonic voluntarydorsiflexion or plantar flexion of the foot. The test stimuli wereapplied every 3--4 s. An interstimulus interval of mo re tha n 10 s hasbeen reco mmended to avoid cumulative depression of the H-reflexby preceding stimuli (Desmedt 1973). But since a longer inter-stimulus interval would result in an unfavourable anticipation ofthe electrical shocks (Yanagisawa 1980) and require an unfavour-ably long period for the experiment, we adopted the presentinterval as a reasonable compromise. The first several reflexes ineach session of the experiment were discarded to minimize thechange in cumulative effect of in hibition by t he pr eceding stimuli.Preceding conditioning stimuli were combined with them inrandom sequences st) that the subject could not anticipate whenthe conditioning stimuli were to be applied. The conditioned H-reflex of the soleus muscle was first recorded with differentconditioning -test stimulus intervals from 0 to 20.0 ms in orde r toreveal the time-course of the conditioning effect. Then, to studythe change of the conditioned H-reflex with respect to the strengthof voluntary dorsiflexion or plantar flexion, recordings were madewith a fixed conditioning-test stimulus interval set bet ween 1.0 and2.0 ms, which showed optimal effect. The threshold of theconditioning stimulus was checked during voluntary" contractio n aswell as at rest, and was verified to be constan t. The size of the testreflex was measured by peak-to-peak amplitude in earlier experi-ments, but in later experiments the H-reflex was subjected to full-wave rectification and integration, and its size was then read outthrough a digital voltmet er. Evo ked E MG re sponses were alsorecorded on an ink-writer through a memory device (8-bit A/I)input, l k words, Kawasaki Electronica TM-1410), the samplingtime and the readout time being 100 las/word and 2 ms/word,respectively, and were used for checking stability in the experi-ment.The muscle contraction was performed nearly isometrically inorder to minimize the change of muscle length. Although the legwas fixed to the immobile foot-plate, the contraction was notcompletely isometric and the angle of the foot could change up toabout 5 deg at the maximal dorsiflexion or plantar flexion.However, the angle-change in actual experiments (up to 30% ofthe maximal contract ion) was much smaller, and did not seem toaffect the results seriously. The amount of contraction wasmonitored by the torque met er and was expressed as a percentageof the torque force at the maximal contraction. The subject wasrequested to adjust the strength of contraction in several degrees,which were indicated on the monitor oscilloscope as a target line.The amount of contraction requested was within 30% of themaximum for the following reasons: (1) The antagonist stretchfrom incomplete fixation of the leg, although inevitable, should beminimized during voluntary contraction. (2) Co-contraction of theantagonists could occur with stronger contraction. (3) Tile uncon-ditioned control H-reflex might decrease very much in size withstronger contraction of pretibial muscles, which would make itdifficult to assess the conditioning effects. (4) The subject wassometimes unable to maintain stronger contraction for a longenough period of time. (5) Relative linearity between EMG andtorque was well maintained in this range.Since the torque is a parameter of the force applied mechani-caUy to the foot-plate we were uncertain whether it would directlyrepresent the physiological phenomenon. To examine the rela-tionship between the mechanical effect and the physiologicalphenomenon, we compar ed the electromyogram of the lower legand the torque around the ankle. In all subjects the amount ofcontraction measured by the torque meter related almost linearlywith that measured by the integrated EMG in the range below40% of the maximal contraction measured by torque, which wasthe range used in the present study. The slope of the regressionline differed somewhat between dorsiflexion and plantar flexion,and among the subjects. Co-contraction of the antagonists was not


3/9

402 M. Shindo et al. : Changes in Reciprocal Ia Inhibition During Voluntary Contraction in Mandem onstrated in the presen t series beyond potential spread fromthe antagon ists.I t took one to two hours for one series of experiments persubject, during which time the laboratory was kept qu iet and thelighting constant. We tried to keep the su bject alert as we ll asrelaxed, and to keep his posture constant throughout the record ingsession.

- - ~ 1 2 0 [

+ 6 (2 "" '"" 1"oN ~ ..........o~ 4o c o n t r o l O 0 ' . 5 1 : 0 1 . 5 2 . ' 0 1 5 3 ' . 0 3 . 5 4 ' . 0C o n d i ti o n i n g - te s t s t im u l u s in t e r v a l ( m s )Fig. 2. Ti me course of Ia inhibition. At rest inhibition beganbetween 1.0 and 1.5 ms after the co nditioning stimulus (filledcircles). The amount of inhibition increased during dorsiflexion(open circles), and alm ost disappeared during plantar f lexion(diamonds). Both contractionswere 5% of the m aximum. A singleconditioning stimulus with intensity of 1 .00 XMT was used. Eachsymbol represents the mean and vertical bars show the standarderror obta ined from 5 to 13 tr ials. The abscissa shows theconditioning-test stimulus interval (ms), a nd the ordinate the sizeof H-reflex (% of the unconditioned value)

R e s u l t s

F i g u r e 2 s h o w s t h e t i m e c o u r s e o f t h e e a r l y su p p r e s -s i o n o f t h e s o l e u s H - r e f l e x b y c o n d i t i o n i n g s i n g l es t i m u l i w i t h a s t r e n g t h j u s t l i m i n a l f o r t h e d i r e c t M -r e s p o n s e o f t h e t ib i a l is a n t e r i o r m u s c l e i n o n e s u b -j e c t .

I n a re s t i n g s t a t e t h e H - r e f l e x b e g a n t o b es u p p r e s s e d a t a c o n d i t i o n i n g - t e s t s t i m u l u s i n t e r v a lb e t w e e n 1 . 0 a n d 1 , 5 m s , t h e m a x i m a l a m o u n t o fs u p p r e s s io n b e i n g 1 9 . 5 % o f t h e u n c o n d i t i o n e d v a l u eo f t h e H - r e f l e x a t 2 . 0 m s ( f il l e d c i r c le s ) . T h i s s u p p r e s -s i o n w a s d e m o n s t r a t e d e v e n w i t h a s t r e n g t h o f 0 .9X M T . T h e c h a r a c te r i st i cs o f s h o r t l a t e n c y a n d l o wt h r e s h o l d ( l es s t h a n 1 X M T ) i n d i c a t e t h a t t h e s u p -p r e s s i o n i s r e c i p r o c a l I a i n h i b i t i o n ( M i z u n o e t a l .1 9 7 1 ; T a n a k a 1 9 7 4 ) . T h i s I a i n h i b i t i o n o n s o l e u sm o t o n e u r o n e s a t r e s t w a s o b s e r v e d i n f o u r s u b j e c t so u t o f f iv e i n c o n t r a s t to t h e p r e v i o u s s t u d y ( T a n a k a1 9 7 4 , 1 9 8 0) , w h i c h s h o w e d a v e r y l o w i n c i d e n c e o f I a

i n h i b it i o n i n n o r m a l p e r s o n s . T h e a m o u n t o f i nh i b i-t i o n , h o w e v e r , d i f f e r e d a c c o r d in g t o o c c a s i o n e v e n i nt h e s a m e s u b j e c t . F o r e x a m p l e , i n t h e s u b j e c t s h o w ni n Fi g . 2, t h e a m o u n t s o f I a in h i b i t i o n ( m e a n v a l u e )b y a s i n g l e c o n d i t i o n i n g p u l s e w i t h c o n d i t i o n i n g - t e s ts t im u l u s in t e r v a l o f 2 . 5 m s w e r e 2 0 . 8 % , 1 9 . 4 % a n d1 1 . 0 % o f t h e c o n t r o l H - r e f l e x i n t h e f i rs t , s e c o n d a n dt h i rd s e s s io n s o f e x p e r i m e n t , w h i c h w e r e c a r r i e d o u ta t i n t er v a ls o f m o r e t h a n o n e m o n t h . G e n e r a l l y th ea m o u n t o f in h i b i t i o n a t r e s t w a s r a t h e r s m a l l , a n dt e n d e d t o d e c r e a s e w i t h r e p e t i t i o n o f e x p e r i m e n t s .T h e m a x i m a l a m o u n t o f i n h i b i ti o n a t r e st a m o n g t h ef o u r s u b j e c t s w a s 1 4 . 4 ___ 5 . 0 ( m e a n a n d S D ) % o f t h ec o n t r o l H - r e fl e x .

D u r i n g t o n i c d o r s i f l e x i o n o f t h e f o o t t h i s i n h i b i -t i o n b e c a m e m o r e r e m a r k a b l e . I n t h e c a s e s h o w n i nF i g. 2 , t h e a m o u n t o f i n h i b i ti o n i n c r e a s e d f r o m1 9 . 5 % t o 5 1 . 1 % o f it s u n c o n d i t i o n e d v a l u e a t 2 .5 m sc o n d i t i o n i n g - t e s t s ti m u l u s i n t e r v a l ( o p e n c i r c le s ) , b u ti t a l m o s t d i s a p p e a r e d d u r i n g t o n i c p l a n t a r f l e x i o n( d i a m o n d s ) . W e e x a m i n e d t h e r e la t i o n s h i p b e t w e e nt h e a m o u n t o f in h i b i t i o n o f t h e c o n d i t i o n e d H - r e f l e xa n d t h e a m o u n t o f t o n i c v o l u n t a r y d o r s i f le x i o n a n dp l a n t a r f l e x i o n . F i g u r e s 3 a n d 5 a r e d a t a f r o m t h es u b j e c t i n F i g . 2 .

I a I n h i b it i on o n A n k l e E x t e n s o r s D u r i n g T o n i cC o n t ra c ti o n o f A n k l e F l e x o rs

F i g u r e 3 sh o w s t h e p e r o n e a l i n h i b i t o r y e f f e c t t e s t e da t t h e o p t i m a l i n t e r v a l o f 2 .0 m s , w h i l e t h e s t r e n g t h o fa n k l e d o r s i f l e x i o n w a s s e t a t s e v e r a l d i f f e r e n t s t a g e s.T h e s iz e o f t h e c o n d i t i o n e d H - r e f l e x e x p r e s s e d a s ap e r c e n t a g e o f i ts u n c o n d i t i o n e d c o n t r o l v a l u ed e c r e a s e d i n p a r a ll e l w i th t h e a m o u n t o f to n i cv o l u n t a r y d o r s i fl e x i o n f r o m 8 8 . 8 % a t r e s t t o 5 1 . 5 % ,2 5 . 2 % , 2 3 . 3 % a s t h e a m o u n t o f c o n t r a c t i o ni n c re a s ed b y 1 0 % , 2 0 % , 3 0 % o f t h e m a x i m u m ,r e s p e c t i v e l y ( F i g . 3 A , o p e n c i r c l e s ) . A t f i r s t s i g h t ,t h i s m i g h t s e e m t o i n d i c a t e t h a t I a i n h i b i t i o n o f s o l e u sm o t o n e u r o n e s i n c r e a s e d i n a c c o r d a n c e w i t h t h es t re n g t h o f v o l u n t a r y d o r s i f le x i o n . H o w e v e r , t h ec o n t r o l H - r e f l e x i t s e l f a l s o d e c r e a s e d i n s i z e d u r i n gd o r s if le x i o n : f r o m 2 5 . 6 % o f th e m a x i m a l M - r e s p o n s ea t r e s t t o 9 . 9 % , 7 . 7 % , 8 . 9 % a t 1 0 % , 2 0 % , 3 0 % o ft h e m a x i m a l c o n t r a c t i o n ( F i g . 3 A , f i l l e d c i r c l e s ; s e ea l s o T a n a k a 1 9 7 4 ). I f t h e s i ze s o f t h e c o n t r o l H - r e f l e xw e r e m a r k e d l y d i f f e re n t , t h e s a m e i n h i b i t o r y e f f e c tc o u l d r e su l t i n d i f fe r e n t a m o u n t s o f c h a n g e , a n d i tw o u l d b e d i f f ic u l t t o c o r r e l a t e d i r e c t l y t h e r e l a t i v ea m o u n t o f i n h i b it i o n , a s e x p r e s s e d b y a p e r c e n t a g e o fi t s u n c o n d i t i o n e d H - r e f l e x , w i t h t h e s t r e n g t h o fc o n t r a c t io n . F o r t u n a t e l y , i n th i s c a se , t h e c o n t r o l H -r e f l e x e s w e r e a l m o s t t h e s a m e a t v a r i o u s s t r e n g t h s o f


4/9

M. Shindo et al.: Changes in Reciprocal Ia Inhibition During Voluntary Contraction in Man 403A B A

" 1 -

! , o t~ - 6 ot~~50-~ 4 0 - 40" r '30~ 8 2 0 i 2 0-510co I I I I Irest 10 20 3 0 reststtn~

"~ 20

8"6

-5

10

YIrest 10

i

I I20 30 res tstknlAm ount o f d ors i f lex ion (% of max.cont r. )

Fig. 3A, B. Inhibition of H-reflex during dorsiflexion. A O p e ncircles show the inhibition, expressed as % of the unconditionedcontrol H-reflex, which increased as contraction strengthened.Filled circles show the control H-reflex, expressed as % of themaximal M-response, which decreased on contraction. When asmaller test H-reflex was used, the inhibition did not increase(right-hand side). Each symbol represents the mean of five dataand the standard error. B The abohite amount of inhibition (% ofM max), which was calculated by subtracting the mean size of theconditioned H from that of the control H, increased in parallelwith the amount of contraction. Each vertical strip indicates therange of expected standard deviation of the difference of means

~3oi- -OO,,- 20O

4

B/1 5E"6c' -.E"65

I I Irest 10 200 I I I d Ir es t 10 20 30 30A mo un t o f do r s i f l ex ion ( % o f m ax . con t r . )

Fig. 4A, B. The change in the control H-reflex size (A) and theabsolute amount of Ia inhibition (B) at rest and during tonicdorsiflexion of the foot in all subjects. The absolute amount o finhibition was calculated as in Fig. 3B. The control H-reflexdecreased in size and the Ia inhibition increased with respect to theamount of contraction. The strength of conditioning stimuli wasbetween 0.9-1.2 XMT. The abscissa shows the amount of contrac-tion (% of the maximum), and the ordinate the size of the controlH-reflex (% of M max, A) and the absolute amount of inhibition(% of M max, B). * and A show the data from the same twosubjects examined on different dates

contraction and, therefore, the increase of inhibitionat stronger contraction, particularly from 10% to20%, seems meaningful. Further, even when weakerstimuli were used at rest so as to obtain the same sizeof test reflex as used during contraction, the amountof Ia inhibition was very small, as was the case in thelarger control H-reflex at rest (compare left-hand andright-hand sides in Fig. 3A). It seems justifiable,therefore, to think that the activity of the Ia inhibi-tory pathway increases as the contraction becomesstronger.

However, the unconditioned H-reflex did notalways remain constant at different amounts ofantagonist contraction. In fact, in the majority ofexperiments, the control H-reflex tended to bedepressed in parallel with the amount of dorsiflexion;the stronger the contraction, the smaller the size ofthe H-reflex (Fig. 4A). Thus, we cannot readilycompare the relative value of inhibition expressed asa percentage of its control value between the restingstate and various stages of contraction. In this case,the size of test H-reflexes could be adjusted at rest tobe the same as that in different experimental condi-tions; i.e. during tonic voluntary contraction. This

procedure, however, has some disadvantages. Forinstance, the detailed shape of the H-reflex duringactive dorsiflexion is not necessarily the same as thatof the H-reflex at rest even if the sizes of the two areadjusted so as to be the same. This means that thesampled motoneuro nes in the test H-reflexes in bothconditions would be partly different. Besides, it takesmuch time to adjust on each occasion the size of thecontrol H-reflex at rest to the same amplitude as invarious strengths of contraction.

We, therefore, decided to calculate the absolutesize of soleus motoneurones that were inhibited bythe conditioning stimuli. This was done by subtract-ing the mean value of the absolute size of theconditioned H-reflex from that o f the unc onditionedcontrol H-reflex, and expressing this as a percentageof the maximal M-response. The value calculated bythis procedure represents the absolute size of moto-neurones which were inhibited by the conditioningvolley within the mo tone urone s partially inhibited bydorsiflexion. Here we call this value the absoluteamount of Ia inhibition. The results were an increasein the absolute amount of Ia inhibition by increaseof dorsiflexion (Figs. 3B and 4B). Figure 3B demon-


5/9

404 M. Shindo et al . : Changes in Reciprocal Ia Inhibition During Voluntary Contraction in Mans t r a t e s a s u c c e s s i v e i n c r e a s e i n i n h i b i t io n f r o m 3 . 0 %a t r e st t o 4 . 8 % , 5 . 7 % , 6 . 8 % o f t h e m a x i m a l M -r e s p o n s e a t 1 0 % , 2 0 % , 3 0 % o f m a x i m a l d o r s if l e x io n ,r e s p e c t i v e l y .

It should be noted that this procedure is apparently anunderestimation of the excitabili ty change in the Ia inhibitorypathway, for the following reasons. Firstly, the soleus moto-neurones, w hich provided p art of the control H -reflex at rest andwere suppressed by active dorsiflexion (Figs. 3A, 4A ), would bemore susceptible to inhibition, including Ia inhibition, than theones suppressed b y the conditioning volley. If this is the case, theformer group of motoneurones were already excluded from thetest sample during contraction, and did no t contribute to the partsuppressed further by a conditioning volley, resulting in a smallerestimation of Ia inhibition than actually occurred. Secondly,increase in Ia discharges from the ankle flexors during activedorsiflexion (Vallbo 1 970) might cause an o cclusion in the afferentpathway, and reduce the size of conditioning I a volleys and thus o fIa inhibition. Since the Ia discharges increase more in strongercontraction (Vallbo 1 974), this factor would play a larger role instronger contractions.F i g u r e 4 s u m m a r i z e s t h e c h a n g e i n si z e o f t h e

u n c o n d i t i o n e d c o n t r o l H - r e f le x ( A ) a s w el l as t h ea b s o l u te a m o u n t o f I a i n h i b it i o n b y t h e c o n d i t i o n i n gs t im u l i ( B ) a t r e s t a n d d u r i n g t o n i c d o r s i f l e x i o n i n a lls u b j ec t s . A l t h o u g h t h e c o n t r o l H - r e f l e x d e c r e a s e d i ns iz e as c o n t r a c t io n s t r e n g t h e n e d , t h e a b s o l u t ea m o u n t o f Ia i n h ib i t io n i n c r e a s e d a l m o s t p a r a l le l w i t ht h e a m o u n t o f c o n t r a c ti o n . T h i s i n d i c at e s a n a c t u a li n c r e as e i n t h e s o le u s m o t o n e u r o n e s w h i c h w e r ei n h i bi t e d v i a t h e I a i n h i b it o r y p a t h w a y a s t h e c o n t r a c -t i o n i n c r e as e d . E v e n t h o u g h t h e i n c r e a s e d a m o u n t o fi n h i b i t io n b y d o r s i f l e x i o n c o u l d c h a n g e i n d i f f e r e n ts e ss i on s d o n e o n d i f f e r e n t d a y s w i t h t h e s a m e s u b -j e c t , th i s r e la t i o n s h i p w a s p r e s e r v e d ; t h is is p r e s e n t e di n F ig . 4 B a s a p a r a l l e l s h i f t o f a l i n e i n t w o s u b j e c t s ,a n d s h o w s t h e r e p r o d u c b i l i t y o f t h e e x p e r i m e n t .

Ia Inhibition on Ankle Extensors During TonicContraction of Ankle ExtensorsF i g u r e 5 s h o w s t h e r e s u l t s f r o m a c a s e i n w h i c h t h ea m o u n t o f i n h i b it i o n o f t h e c o n d i t i o n e d H - r e f l e xd e c r e a s e d f r o m 5 0 . 1 % o f i ts u n c o n d i t i o n e d v a l u e a tr es V to 9 . 4 % , - 2 . 9 % , 0 . 3 % a t a m o u n t s o f c o n tr a c ti o n ,o f 10 % , 2 0 % , 3 0 % o f t h e m a x i m u m ( F ig . 5 A , o p e nc ir c le s ). O n t h e o t h e r h a n d , t h e u n c o n d i t i o n e d c o n -t r o l H - r e f l e x i t s e lf in c r e a s e d s u c c e s s i v e l y f r o m 2 8 . 9 %o f t h e m a x i m a l M - r e s p o n s e a t re s t t o 4 2 . 1 % , 4 3 . 4 % ,4 8 . 0 % a t 1 0 % , 2 0 % , 3 0 % o f t h e m a x i m a l c o n t r a c t i o n( f il le d c ir c le s ) . T h e a b s o l u t e a m o u n t o f i n h i b i t i o n ,w h i c h w a s c a l c u l a t e d a s in t h e s e r ie s o n d o r s i f l e x i o n ,d e c r e a s e d f r o m 1 4 . 4 % a t r e s t t o 3 . 9 % , - 1 . 3 % , 0 . 2 %o f t h e m a x i m a l M - r e s p o n s e a t 1 0 % , 2 0 % , 3 0 % o f t h em a x i m a l p l a n t a r f l e x i o n ( F i g . 5 B ) .

i! 1 o o8 0

i , o [~ac

A

"5 15

. i

B

I I I I I I | Ires t 10 20 30 res t 10 20 30Amount o f p lantar f l ex ion ( o~ o f max . cont r . )

Fig. 5A, B. Inhibition o f H-reflex d uring plantar flexion. Similaril lustration as Fig. 3. A The inhibition decreased, while the controlH-reflex increased as voluntary contraction strengthened. B Th eabsolute amount of inhibition decreased in parallel with them ou n t o f cont rac ti on

w~5 20

A " ~ 1 5E

~1o

~5 5

0 I I I= , Ires t 10 2 O 3OA m oun t o f p l an t a r f lex i on

B

I I I Ir e s t 10 20 30( % o f m ax . c on t r . )

Fig. 6A, B. The change in the control H-reflex (A) and theabsolute amount of Ia inhibition (B) at rest and during tonicplantar flexioff'in all subjects. Similar iUustr~ion as Fig: 4. Thecontrol H-reflex increased in si ze during contraction, and theabsolute amount of Ia inhibition decreased almost parallel with theamount o f contraction. The stimulating condition was the same asin Fig . 4

F i g u r e 6 s u m m a r i z e s t h e c h a n g e o f th e c o n t r o l H -r e fl e x a n d t h e a b s o l u t e a m o u n t o f in h i b i ti o n w i t hr e s p e c t t o t h e a m o u n t o f to n i c p l a n t a r f l e x i o n in al lf i v e s u b j e c t s . T h e c o n t r o l H - r e f l e x i n c r e a s e d i n s iz ew i th s t r o n g e r v o l u n t a r y c o n t r a c t i o n , a n d a t t h e s a m e


6/9

A

a m o u n t o fl a i n h i b i t i o n

o o o o o o o o o 9o o o o e o o o o o o o o

o o o o eo o o o o o o o o o o. o o , o o , o o * o o o % o o ~eo eo o o o o eo o eo ~ 9o o o o o o o o o o o o o o o o oo o o o o o o eeo o o o o o o eo o o o o o o o o o o o o ~o oo o o o o o o o o o o o o o oo o o o o o o eo o o ~o oo o o o o o o o o o o o oo o o o o o o o o o o o oo o o o o o o o o o o oo o o o o o oo o o o o o o o ooo9 OoOo~o o~ o

M. Shindo et al.: Chan ges in Reciproc al Ia Inhibition During Volun tary Con traction in Man 405B[ d ~ i I = f k o , I

Fig. 7. A Schem atic llustration of the relationship between the amo unt of Ia inhibition (ordinate)and the amount of contraction(abscissa) based on the present data. The excitabilityof Ia inhibitory pathway changes continuously rom dorsiflexion hrough restto plantar fexion. B Neu ronal connection concerning reciprocal Ia inhibition. For explanation s see text. (E , ex citation; I,inhibition; ct, ct moton eurone; y, ? moto neurone ; Ia, Ia inhibitory interneurone; R, Rensha w cell)

t i m e t h e a b s o l u t e a m o u n t o f I a i n h i b it i o n d e c r e a s e da l m o s t i n p a r a l l e l w i th t h e a m o u n t o f c o n t r a c t i o n . I no n e e x c e p t i o n a l s u b j e c t ( i n d i c a t e d b y a n a s t e r i s k ) ,t h e a m o u n t o f i n h i b it i o n i n c r e as e d d u r i n g p l a n t a rf l e x i o n a s w e l l a s d o r s i f l e x i o n , b u t n o c o - c o n t r a c t i o no f p re t ib i a l m u s c le s w a s d e m o n s t r a t e d d u r i n g p l a n t a rf l e x i o n .

D i s c u s s i o nI a I n h i b i t io n a t R e s tT h e I a i n h i b i ti o n o f e x t e n s o r s o le u s m o t o n e u r o n e sf r o m t h e f l e x o r n e r v e w a s r e v e a l e d a t r e s t in f o u rs u b j e c t s o u t o f f iv e in t h e p r e s e n t s t u d y . T h e r e l a -t i v e ly h ig h i n c i d e n c e o f I a i n h i b i t i o n a t r e s t isn o t e w o r t h y , b e c a u s e i t w a s p r e v i o u s l y r e p o r t e d t oh a v e b e e n r e c o g n i z e d o n l y i n a f e w n o r m a l s u b j e c t s( M i z u n o e t a l . 1 9 7 1 ; T a n a k a 1 9 7 4 , 1 9 8 0 ) . O n e f a c t o ri n th e h i g h i n c i d e n c e o f Ia i n h i b i t i o n i n t h e p r e s e n t

s t u d y c o u l d b e t h a t th e p r e s e n t e x p e r i m e n t w a s d o n eo n s u b j e c t s s i t t i n g i n a c h a i r , w h i l e t h o s e i n t h ep r e v i o u s e x p e r i m e n t s w e r e c a r r i e d o u t i n t h e p r o n ep o s i t i o n . I n th e l a t t e r s i t u a t i o n t h e s u b j e c t ' s k n e e w a si n a n a l m o s t e x t e n d e d p o s i t i o n , w i t h t h e f o o t p r o t -r u d i n g fr e e l y f r o m t h e e d g e o f t h e b e d a n d t h u s b e i n gp u l le d d o w n w a r d s s o m e w h a t b y t h e f o r c e o f g r a v it y .T h i s p o s i t i o n n a t u r a l l y c a u s e s a c e r t a i n s t r e t c h i n go f th e t r i c e p s s u r a e m u s c l e , w h i c h c o u l d r e s u l t i nf a c i l i t a t i o n o f e x t e n s o r I a i n h i b i t o r y i n t e r n e u r o n e sv i a i n c r e a s e d e x t e n s o r I a d i s c h a r g e s a n d l o w e r t h ee x c it a b il i ty o f t h e f e x o r I a i n h i b i t o r y p a t h w a y .A n o t h e r f a c t o r t o b e c o n s i d e r e d i s t h a t a l l t h es u b j e c t s w e r e y o u n g a n d a t h l e t i c a n d s h o w e d m i l dt o m o d e r a t e h y p e r r e f l e x i a b y t e n d o n t a p i n th el o w e r e x t r e m i t i e s ; i n s o m e s u b j e c t s t h e H - r e f l e x w a sd e m o n s t r a t e d e v e n i n p r e t i b i a l m u s c l e s a t r e s t .T a n a k a ( 1 9 7 4 ) d i s c e r n e d I a i n h i b i t i o n o n t h e a n k l ee x t e n s o r m o t o n e u r o n e s f r o m t h e f l e x o r s a t r e s t i no n e s u b j e c t in w h o m t h e H - r e f l e x w a s d e m o n s t r a t e di n p r e t i b i a l m u s c l e s , a n d h e d i s c u s s e d t h e s h i f t i n


7/9

406 M. Shindo et al.: Changes in Reciprocal Ia Inhibition During VoluntaryContraction n Manequiliblium between the ankle flexor and extensorexcitabilities to the flexor side. Since Ia inhibition atrest was recognized most clearly in the first session ofexperiment in the present study, the psychologicalfactor should not be disregarded either. Although Iainhibition was observed at rest in most subjects, themaximal amount of inhibition was small and the in-hibition itself disappeared readily on plantar flexionand also tended to become less clear with repetitionof experiments in all the subjects.

Quanti ta t ive Evaluat ion o f la Inhibi t ion at Res tand During Tonic Voluntary Contrac t ionIa inhibition on soleus motoneurones was demon-strated during dorsiflexion of the foot in all subjects,which confirms the results in a previous report(Tanaka 1974). Furthermore, the present study dis-closed a quantitative relationship between theamount of inhibition and the amount of voluntarycontraction. The absolute amount of soleus moto-neurones which were inhibited by the conditioningvolley increased during dorsiflexion and decreased ordisappeared during plantar flexion, in parallel withthe amount of tonic voluntary contraction.As the conditioning effect on the H-reflex mayvary according to the size of the test H-reflex(Desmedt 1973), it was imperative to examinewhether a smaller H-reflex might reveal a larger Iainhibition in the present study. There was no virtualincrease of Ia inhibition at rest when tested on asmaller H-reflex (Fig. 3A, right-hand side). On theother hand, it was disclosed (Kuno 1959) in arelationship between the size of the test monosynap-tic reflex and its recurrent inhibition in the spinal cat,that the amount of inhibition by the same recurrentvolley increased as the tes t reflex increased its size upto 40% of the total motoneurone pool. The effectremained constant thereafter up to 65% of the testsize (Fig. 2 in Kuno 1959). In the present study, thesize of the test H-reflex was expressed as a percen-tage of the maximal M-response, which is the sameprinciple as Kuno's method, and it was less than 60%of the maximal response. Although it is uncertainwhether the relationship between the size of mono-synaptic reflex and the amoun t of inhibition might beapplied to the Ia inhibition in man or no t, the presentstudy showed that the amount of Ia inhibitionincreased in spite of a decrease in test H-reflex sizeduring dorsiflexion, which is in the opposite directionfrom Kuno's results. We may conclude that the Iainhibitory pathway from ankle flexor to extensor isfacilitated during tonic voluntary dorsiflexion and isdepressed during voluntary plantar flexion, in

accordance with the amount of contraction. This isthe main finding disclosed in the present study.

The Neural Mechanisms Control l ingla Inhibi tory PathwayThere are several known mechanisms which controlthe excitability of the Ia inhibitory pathway. Twopossible mechanisms of increase in la inhibitionduring dorsiflexion can be considered; (1) facilitationof Ia inhibitory interneurone directly by descendingroutes and/or indirectly by increased activity of Iaafferents by way of the ~,-loop, and (2) disinhibitionof Ia interneurone by inhibition of Renshaw-cellactivity. Figure 7B shows the neuronal connectionsfor these mechanisms. The first mechanism, which isproperly described as the "ct-~/-linkage in reciprocalinhibition" (Hongo et al. 1969; Lundberg 1970), hasbeen discussed in detail elsewhere (Tanaka 1974,1976). In brief, the reciprocal Ia inhibitory inter-neurone is facilitated directly from supraspinal struc-tures, e.g. the corticospinal tract in the monkey(Jankowska and Tanaka 1974; Jankowska et al.1976). Such a descending facilitation was demon-strated indirectly in human experiments combinedwith voluntary movements (Simoyama and Tanaka1974). Another source which facilitates Ia inter-neurones is group Ia afferents from homonymousand synergistic muscles. These afferents have beenshown in human experiments to increase in dis-charge-frequency during isometric volunta ry contrac-tion (Vallbo 1970). Vallbo further showed that thefrequency increased as the contraction intensified(Vallbo 1974). These observations would suggestthe first mechanism to be the most likely one. Con-cerning the second possible mechanism, since theRenshaw cell has inhibitory connection to the Iainhibitory interneurone (Hultborn et al. 1971), thelatter's activity can be facilitated by suppression ofthe former. Although the strongest excitatory inputso far known for the Renshaw cell is the axon-collateral of the ct motoneurone, the Renshaw cell isalso under control of segmental or supraspinal cen-ters (cf. Baldissera et al. 1981). Recently the excita-bility of the recurrent inhibitory pathway in man hasbeen investigated during voluntary contraction withan indirect method (Hultborn and Pierrot-Deseil-ligny 1979). The investigators demonst rated thatduring tonic plantar flexion the excitability ofRenshaw cells on the agonist side decreased progres-sively in 40%, 60% and 80% of the maximal contrac-tion, and they suggested that this decrease would bedue to an inhibitory control (spinal and/or supra-segmental) acting on Renshaw cells and would be


8/9

M. Sh in d o e t a l . : Ch an g es in Rec ip ro ca l I a In h ib i t io n Du r in g Vo lu n ta ry Co n t rac t io n in Man 4 0 7f av o u r ab l e f o r r ec i p r o ca l I a i n h i b i t i o n ( s ee F i g . 7 B ) .H o w e v e r , t h e y c o u l d n o t s h o w s u c h i n h i b i t i o n o fR en s h aw - ce l l a c t i v i t y d u r i n g w eak co n t r ac t i o n( 1 0 % ) . F u r t h e r m o r e , i t i s u n k n o w n w h e t h e r t h i s i sa l s o t h e ca s e i n t h e f l ex o r R e n s h a w ce l ls d u r in g t o n i cd o r s if l ex io n . T h e p r e s en t s t u d y w as p e r f o r m ed o nr a t h e r w e a k c o n t r a c t io n b e t w e e n 5 a n d 3 0 % o f t h em ax i m a l f o r ce , an d n o q u a l i t a t i v e d i f f e r en ce i n t h ei n c r ea s e o f I a i n h i b i ti o n w as o b s e r v e d i n t h is r an g e .T h e r e f o r e , w e t e n t a ti v e l y s u g g e st t h a t t h e R e n s h a w -ce l l m ech an i s m w o u l d n o t co n t r i b u t e m u ch t o f ac i l i -t a t io n o f t h e I a i n h i b i to r y p a t h w a y d u r i n g w e a k e rd o r s i f l ex i o n a s i n t h e p r e s en t s t u d y . S o m e co n t r i b u -t i o n f r o m t h e R e n s h a w - c e l l m e c h a n i s m w o u l d b eex p ec t ed a t a s t r o n g e r co n t r ac t i o n .

T h e d ec r ea s e i n ex c i t ab i l i t y o f t h e I a i n h i b i t o r yp a t h w ay d u r i n g t o n i c p l an t a r f l ex i o n ( F i g s. 5 an d 6 )w o u l d b e e x p l a i n e d m o s t s i m p l y b y t h e i n hi b it io n o fI a i n t e r n eu r o n es o n t h e f l ex o r s i d e b y I a i n t e r -n eu r o n es o n t h e ex t en s o r s i d e , w h i ch w as f ac i l i t a t edi n t h e s am e w ay a s t h e f l ex o r I a i n t e r n eu r o n e s d u r i n gd o r s i fl ex i o n d e s c r i b ed ab o v e ( F i g . 7 B ) . I n t h e ca t , I ai n h i b i t o r y i n t e r n eu r o n es r ece i v e d i s y n ap t i c I P S Pf r o m I a a ff e r en t s fr o m t h e a n t ag o n i s t ( H u l t b o r n e t a l.1 9 7 1 ) , an d t h i s m ay a l s o b e t r u e i n m an . A n o t h e rp o s s i b il i ty , w h i ch r em a i n s t o b e d em o n s t r a t e d , i s t h a tt h e I a i n h i b i t o r y i n t e r n eu r o n e i s i n h i b i t ed o r d i sf aci li -t a t ed d i r ec t ly b y s u p r a s p i n a l c en t e r s d u r i n g an t ag o -n is t con t r ac t ion .

Functional Signif icance o f ReciprocalIa Inhibitory P athwayTan aka (1974 , 1976) sugge s ted a c lose para l le l i smb e t w een t h e ex c i t ab i li t y o f ag o n i s t t~ m o t o n e u r o n esan d t h e ex c i t ab il i ty o f t h e I a i n h i b i t o r y p a t h w ay t ot h e an t ag o n i s t . H e a l s o d i s cu s s ed ex t en s o r p r ed o m i -n an ce i n t h e ex c i t ab i l it y b a l an c e b e t w e en f l ex o r s an dex t en s o r s o f t h e f o o t f r o m t h e r e s u l t s o n I a i n h i b i ti o n .T h e p r e s e n t r e s u l t p r o v i d es f u r t h e r s u p p o r t t o t h is . I nn o r m a l m a n e x t e n s o r p r e d o m i n a n c e e x i s t s , a s t h eam o u n t o f I a i n h i b i ti o n f r o m f l ex o r t o ex t en s o r a t r e s tw a s n o t s o m a r k e d a n d t h e r e w a s n o c o n s t a n t H -r e f lex i n p r e t i b i a l m u s c l e s . T h e p r e s en ce o f an k l e -j e r k an d f a i l u r e t o p r o v o k e t en d o n - j e r k i n p r e t i b i a lm u s c l e s a r e c o m m o n f i n d i n g s i n n o r m a l m a n t os u p p o r t t h e i d e a o f e x t e n s o r p r e d o m i n a n c e i n Ia -m ed i a t ed m o n o s y n ap t i c r e f l ex i n l eg m u s c l e s . W i t hl e s i o n s i n t h e cen t r a l n e r v o u s s y s t em , t h i s ex t en s o rp r e d o m i n a n c e i n t h e l o w e r e x t r e m i t i e s d e v e l o p sm ar k ed l y , a s i n cap s u l a r h em i p l eg i a i n m an an ddecerebra te r ig id i ty in an imals (Creed e t a l . 1932) .T h u s t h e e x t e n s o r p r e d o m i n a n c e i n th e l e g s e e m s tob e f u n d a m e n t a l i n n e u ra l c o n n e c t i o n s i n b o t h n o r m a l

an d p a t h o l o g i ca l co n d i t i o n s . T h i s i s a p u r p o s e f u l o rev en c r u c i a l n eu r a l m ech an i s m f o r m a i n t a i n i n g as t an d in g p o s i t i o n w i t h t h e s o l e s o f t h e f ee t p l an t ed o nt h e g r o u n d, a n d m u s t h a v e d e v e l o p e d t h r o u g h a l o n gco u r s e o f p h y l o g en es i s a s w e l l a s o n t o g en es i s . F o rv o l u n t a ry m o v e m e n t o f t h e f o o t , h o w e v e r , t h isb a l an ce h a s t o b e a l t e r ed w i t h r e s p ec t t o t h e d i r ec t i o nas w e l l a s t h e am o u n t o f m o v em en t . T h i s a l t e ra t i o nco u l d b e ach i ev ed a t l e a s t p a r t l y b y co n t r o l l i n g t h eex c i t ab il i ty o f t h e r ec i p r o ca l I a i n h i b i t o r y p a t h w ay i nc o m b i n a t i o n w i t h a g o n is t a m o t o n e u r o n e s . T h er e s u lt s o f t h e p r e s e n t s t u d y m ay p r o v i d e a p h y s i o l o g i -ca l b a si s f o r t h is m ech an i s m .Acknowledgement. The au th o rs wish to ex p re s s th e i r th an k s to Mr .P .E . Dav en p o r t fo r s c ru t in iz in g th e i r En g l i sh .

References

Bald i s se ra F , Hu l tb o rn H , I l l e r t M (1 9 8 1 ) In teg ra t io n in sp in a ln eu ro n a l sy s tems . In : Bro o k s V (ed ) Ha n d b o o k o f p h y s io l-o g y , Sec t io n I : Ne rv o u s sy s tem I I . Amer ican Ph y s io lo g ica lSocie ty , Bethesda, pp 509-595C r e e d R S , D e n n y - B r o w n D , E c c l e s J C , L i d d e l E G T , S h e r r in g t o nCS (1 9 3 2) R e f lex ac t iv ity o f th e sp in a l co rd . R ep r in ted wi than n o ta t io n s b y Llo y d DPC (19 7 2) O x fo rd Un iv e rs i ty Pre ss ,Lo n d o n , p p 1 4 8 -1 5 1Desm ed t JE (1 97 3 ) A d i scu ss io n o f th e me th o d o lo g y o f th e t r i c ep ssu rae T- an d H- re f lex es . In : Desmed t JE (ed ) New d ev e l -o p men ts in e lec t ro my o g rap h y an d c l in ica l n eu ro p h y s io lo g y ,v o l 3 . Ka rg e r , Base l , p p 7 7 3 -7 8 0l~cd es JC 0 9 6 9 ) Th ~ in h ib i to ry p a th way o f th e cen t ra l n e rv o u ssy s tem. Liv e rp o o l Un iv e r s i ty Pre s s , L iv e rp o o lHo n g o T , J an k o wsk a E , Lu n d b e rg A (19 6 9) Th e ru b ro sp in a l t r ac t .I I . Fac i l i t a t io n o f in te ru eu ro n a l t r an smiss io n in r e f lex p a th s tom o t o n e u r o n e s. E x p B r a i n R e s 7 : 3 6 5 - 3 9 1Hu l tb o rn H , J an k o wsk a E , L in d s t ro m S (1 9 7 1 ) Recu r ren t in h ib i -t io n f ro m ax o n co l la te ra l s o f t r an smiss io n in th e Ia in h ib i to ryp a th way to mo to n eu ro n es . J Ph y s io l (Lo n d ) 2 1 5 :5 9 1 -6 1 2Hu l tb o rn H (1 9 7 2 ) Co n v e rg en ce o n in te rn eu ro n es in th e rec i -p ro ca l I a in h ib i to ry p a th way to mo to n eu ro n es . Ac ta Ph y s io lScand [Suppl] 375:1--42Hu l tb o rn H , P ie r ro t -Dese i l l ig n y E (1 9 79 ) Ch an g es in r ecu r ren t

in h ib i t io n d u r in g v o lu n ta ry so leu s co n t rac t io n s in man -s tu d ied b y an H- re f lex t ech n iq u e . J Ph y s io l (Lo n d ) 2 9 7:229-251Jan k o wsk a E , Tan ak a R (19 7 4) Neu ro n a l mech an ism o f th ed isy n ap t ic in h ib i t io n ev o k ed in p r ima te sp in a l mo to n eu ro n esf ro m th e co r t i co sp in a l t r ac t . Bra in Res 7 5 :1 6 3 -1 6 6Jan k o wsk a E , Pad e l Y , Tan ak a R (1 9 7 6 ) Disy n ap t ic in h ib i t io n o fs p in a l m o t o n e u r o n e s f r o m t h e m o t o r c o r t e x in t h e m o n k e y .J Ph y s io l (Lo n d ) 2 5 8 :4 6 7 -4 8 7Ku n o M (1 9 5 9 ) Ex c i tab i l i ty fo l lo win g an t id ro mic ac t iv a t io n insp in a l mo to n eu ro n es su p p ly in g red mu sc le s . J Ph y s io l (Lo n d )1 4 9 :3 7 4 -3 9 3Lu n d b e rg A (1 9 7 0 ) Th e ex c i ta to ry co n t ro l o f th e Ia in h ib i to ryp a th way . In : An d e rso n P , J an sen JKS (ed s ) Ex c i ta to rysy n ap t ic mech an isms . Un iv e r s i t e t s fo r lag e t , O s lo , p p 3 3 3-34 0Mizu n o Y, Tan ak a R , Yan ag isawa N (1 9 7 1 ) Rec ip ro ca l g ro u p Iin h ib i t io n o f t ri c ep s su rae mo to n eu ro n es in man . J Neu ro -p h y s io l 3 4 :1 0 1 0 -1 0 1 7


9/9

4 0 8 M. Sh in d o e t a l . : Ch an g es in Rec ip ro ca l I a In h ib i t io n Du r in g Vo lu n ta ry Co n t rac t io n in ManSimo y ama M, Tan ak a R (1 9 7 4 ) Rec ip r ica l I a in h ib i t io n a t th eo n se t o f v o lu n ta ry mo v em en ts in man . Bra in R es 8 2 :33 4 --3 37Tan ak a R (1 9 7 4 ) Rec ip ro ca l I a in h ib i t io n d u r in g v o lu n ta ry mo v e -men ts in man . Ex p Bra in Res 2 1 :5 2 9 - -5 4 0Tan ak a R (1 9 7 6 ) Rec ip ro ca l I a in h ib i t io n an d v o lu n ta ry mo v e -men ts in man . In : H o m ma S (ed ) Un d e rs tan d in g o f th e s t r e tchr e f le x . E l s e v ie r , A m s t e r d a m O x f o r d N e w Y o r k ( P r o g B r a inRes , v o l 44 , p p 2 9 1 -3 0 2 )Tan ak a R (1 9 8 0 ) In h ib i to ry mech an ism in rec ip ro ca l in n e rv a t io nin v o lu n ta ry mo v emen ts . In : Desmed t JE (ed ) Sp in a l an dsu p ra sp in a l mech an isms o f v o lu n ta ry mo to r co n t ro l an dlo co mo t io n . Ka rg e r , Base l (Pro g Cl in Neu ro p h y s io l , v o l 8 ,pp 117-128)Va l lb o AB (1 9 7 0 ) Disch a rg e p a t te rn s in h u man mu sc le sp in d lea f fe ren t s d u r in g i so me t r ic v o lu n ta ry co n t rac t io n s . Ac ta Ph y -s io l Scan d 8 0 :5 5 2 -5 6 6

Va l lb o AB (1 97 4 ) Hu m an m u sc le sp in d le d i sch a rg e d u r in g i so me t -r ic v o lu n ta ry co n t rac t io n s . Am p l i tu d e re la t io n s b e tw een sp in -d le f r eq u en cy an d to rq u e . Ac ta Ph y s io l Scan d 9 0 :3 1 9 -3 3 6Yan ag isawa N, Tan ak a R , I to Z (19 7 6) Rec ip ro ca l I a in h ib i t io n insp as ti c h emip leg ia o f man . Bra in 9 9 :5 5 5 -5 7 4Yanagisawa N, Tanaka R (1978) Reciprocal Ia inhib it ion in spast icp a ra ly s is in man . In : Co b b W A, D u i jn H (ed s ) Co n tem p o ra ryc lin ica l n eu ro p h y s io lo g y . E lsev ie r , Am s te rd am (EE G Su p p l ,No 34, pp 521-526)Yan ag isawa N (1 9 8 0 ) Rec ip ro ca l r e f lex co n n ec t io n s in mo to rd i so rd e r s in man . In : D esmed t JE (ed ) Sp in a l an d sup ra sp in almech an isms o f v o lu n ta ry mo to r co n t ro l an d lo co mo t io n .Karg e r , Base l (Pro g Cl in Neu ro p h y s io l , v o l 8 , p p 1 2 9 -1 4 1 )

Rece iv ed Feb ru a ry 2 2 , 1 9 83

Documents

Reciprocal Inhibition Contract Muscle