3-15_Excitability of the Soleus H-Reflex Arc During Walking and Stepping in Man

8/3/2019 3-15_Excitability of the Soleus H-Reflex Arc During Walking and Stepping in Man

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E x p B r a i n R e s ( 19 8 7) 6 6 : 4 % 6 0 E x m e n t a lB r a nR e s e a r c h9 Spr inger-V erlag 1987

Ex c i t a b i l i t y o f t h e s o l e u s H- r e f l e x a r c d u r i n g wa l k i n g a n d s t e p p i n g i n ma n

P. Crenna t and C. F r igo 2

1 I s t it u to d i F is io lo g i a U m an a I I , U n iv e r s i t a d i M i l an o , Via M an g iag a ll i 3 2, 1 -2 0 13 3 M i l an o , I t a ly2 C en t ro d i B io in g eg n er i a - F n d . P ro Ju v en tu t e , P o l i t ecn i co d i M i l an o , V ia G o zzad in i 7 , 1 -20 1 4 8 M i l an o , I t a ly

Summary. In e igh t normal sub jec t s , t he exc i t ab i l i t yo f the so leus (So l ) H- re f l ex wa s t es t ed in pa ra l l e l wi th

So l l eng th changes , EM G s o f l eg and th igh musc lesand g round con tac t phases , du r ing th r ee d i f f e r en tpac ing movement s : b ipeda l t r eadmi l l wa lk ing , s ing lel imb t r eadmi l l wa lk ing , and s ing le - l imb s t epp ing ono n e s p o t. A c o m p u t e r i z e d p r o c e d u r e w a s u s e d w h i c hcompensa ted fo r changes in s t imulus e f f ec t ivenesstha t occur r ed dur ing f r ee mot ion . I n the th r eeparad igms ex amin ed , s ign if i cant exc i t ab i li t y mo du la -t ions were observed wi th r espec t t o a con t ro l l eve lde te rm ined in s t and ing weigh t -bear ing pos i t ion . Dur-ing b ipeda l t r eadmi l l wa lk ing , exc i t ab i l i t y wasdecreased in the ea r ly s t ance , max imal ly enhanced inthe second ha l f o f t he s t ance , and aga in dec reaseddur ing the end - s t ance an d the w hole swing phase ,w i t h a m i n i m u m v a l u e a r o u n d t h e t o e o f f p e r i o d . T h emain modula t ion pa t t e rn was r e t a ined dur ing s ing le -l imb t r eadmi l l wa lk ing . Dur ing s ing le - l imb s t epp ingon one spo t , t he s t ance-phase inc rease in exc i t ab i l i t yand the swing phase depress ion were s t i l l p r esen t .H o w e v e r, i n t h e s e c o n d h a l f o f th e s w i ng p h a s e ,r e f l ex r espons iveness r e tu rned to r e f e r ence l eve l ,w h i c h w a s m a i n t a i n e d d u r in g t h e s u b s e q u e n t c o n t a c tper iod . Moreover, a decrease in r e f l ex exc i t ab i l i t yw a s d e t e c t e d a r o u n d t h e m i d - s ta n c e . T h e t i m e c o u r s eo f t h e d e s c r i b e d m o d u l a t i o n s w a s o n l y p a rt l y c o r r e -

l a t e d w i t h th e E M G a n d l e n g t h c h a n g e s o f t h e S o lm u s c le . F u r t h e r m o r e , i n t h e t h r e e m o v e m e n t s te s t e d ,dur ing the ea r ly s t ance pha se , t he exc i t ab i l i t y o f theH - r e f l e x a r c d i d n o t c o r r e s p o n d t o t h e o n e e x p e c t e don the bas i s o f the ava i l ab le H- re f l ex s tud ies pe r -fo rmed under s t a t i c cond i t ions . I t i s sugges ted tha t ,a t l east in ce r t a in s t r ide phase s ( e .g . a roun d th e ea r lycon tac t pe r iod) , an ac t ive r egu la t ion a f f ec t s t het r ansmiss ion in the So l my ota t i c a r c dur ing the pac ingm o v e m e n t s i n v e st i ga t e d .

Offpr in t reques t s to :P. C ren n a ( ad d res s see ab o v e )

Key words: L o c o m o t i o n - P r o p r i o c e p t i v e r e fl e x e s -H- re f l ex - Sp ina l co rd - Ma n

Introduction

Severa l l i nes o f ev idence , ob ta ined in an imal s f romdi f f e r en t evo lu t ionary phy la , suppor t t he genera lconcep t tha t du r ing locomo t ion , t he cen t r a l p rogramfor the syn thes i s o f t he basa l s t ep synerg ies can a l soac t ive ly r egu la t e r e f l ex t r ansmiss ion bo th in ex te ro -and p ropr iocep t ive pa thways (Ander sson e t a l . 1978 ;S h o m b u rg a n d B e h r e n s 1 9 7 8 ; L e n n a r d a n d H e r m a n -

son 1985 ; see Gr i l lne r 1981 fo r a comprehens iverev iew) . Such a no t ion impl i es tha t t he sameper iphera l i npu t may r esu l t i n qu i t e d i f f e r en t r e f l exr e s p o n se s d e p e n d i n g o n t h e p h a s e o f t h e a f f e re n tvo l l ey wi th in the s t ep cyc le . I t has be en p ro pos ed tha tth i s phenomenon ass i s t s ongo ing musc le con t r ac t ionand p ro tec t s aga ins t po ten t i a l ly pe r tu rb ing r e f l exef f ec t s i n spec i f ic phases o f the s t r ide .

In the l a s t f ew year s , t he f i rs t s tud ies have bee np u b l i s h e d w h i c h h a v e l o o k e d f o r t h e p r e s e n c e o f as imi l a r con t ro l mechan i sm dur ing human ga i t . Asregards ex te rocep t ive r e f l exes , i t was shown tha ts t imula t ion o f cu taneous foo t ne rves a t t ac t i l e i n t en -s i ty can e l i c i t l ow ampl i tude r e f l ex r esponses in l egand th igh m usc les exc lus ive ly during the i r r hy thmiclocom otor ac tiva t ion (Crenna and F r igo 1983 ; Ka ndaand S a to 1983) . By con t r as t , pa in fu l s t imul i t o thesame nerves were found to evoke d i s t inc t phase -r e l a t ed r esponses bo th in f l exor and ex tensor mus-c l es , e v e n in t h e a b s e n c e o f b a c k g r o u n d E M Gact iv ity (Crenna and F r igo 1984; Be lange r and Pa t l a1984) . The poor co r r e l a t ion be tween the t ime cour seof re f l ex changes an d the ac t iva t ion pa t t e rn o f thee f f ec to r musc les wi th in the s t ep cyc le , a s we l l a s thed i f fe r en t i a l mo du la t ion o f the sh or t and long l a t ency


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c o m p o n e n t s o f t h e s a m e r e f l e x r e s p o n s e ( s e e C r e n n aa n d F r i g o 1 9 8 4 ), a r g u e i n f a v o r o f a n a c t i v e a n d q u i t es o p h i s t i c a t e d r e g u l a t i o n a l o n g n o c i c e p t i v e p a t h w a y si n m a n . C o n t r i b u t i o n s f r o m c e n t r a l s y st e m s , p o s s i b l yc o n t r o l l e d b y a c e n t r a l p a t t e r n g e n e r a t o r , b u t a l s of r o m p e r i p h e r a l f e e d b a c k a c t iv a t e d d u r in g m o t i o nm i g h t b e p o s t u l a t e d .

H o w e v e r , t h e d e s c r i b e d e x c i t a b i li t y f l u c t u a ti o n sh a v e b e e n s h o w n f o r r e f l ex r e s p o n s e s m e d i a t e d b yv e r y c o m p l e x a n d p o o r l y k n o w n p o l y s y n a p t i c p a t h -w a y s . A b e t t e r u n d e r s t a n d i n g o f t h e m e c h a n i s m si n v o l v e d w o u l d r e q u i r e a d e t a i l e d s t u d y o f m u c hs i m p l e r r e f l e x c i r c u it s . I n t h i s r e g a r d , t e s t i n g t h eH o f f m a n n r e f le x a rc c o u l d p r o v i d e b a s i c i n f o r m a t i o no n t h e e x c i t a b il i t y l e v e l o f a l p h a m o t o n e u r o n s a n d o fp r e s y n a p t i c i n h i b i t io n a c t i n g o n I a t e r m i n a l s . P r o b -a b l y d u e t o t e c h n i c a l d i f f i c u l t ie s , H - r e f l e x s t u d i e sd u r i n g h u m a n l o c o m o t i o n a r e q u i t e r a r e ( M o r i n e t a l .

1 9 8 2, G a r r e t t e t a l . 1 98 4 ). A n i n c r e a s e i n H - r e f l e xe x c i ta b i l i t y d u r i n g t h e s t a n c e p h a s e a n d a r e d u c t i o nt h r o u g h o u t t h e s w i n g p h a s e w e r e d e s c r i b e d in m e d i a lg a s t r o c n e m i u s ( G a r r e t t e t al . 1 98 4 ). H o w e v e r , i n t h ea v a i l a b le s tu d i e s , t h e t i m e c o u r s e o f H - r e f l e x c h a n g e sw a s a s s e s se d w i th a l o w t e m p o r a l r e s o l u t i o n , o r e v e ni n a l i m i t e d p e r i o d w i t h i n t h e s t r i d e . M o r e o v e r , t h ec o r r e l a t i o n b e t w e e n r e f l ex c h a n g e s a n d r e l e v a n tk i n e m a t ic a n d / o r d y n a m i c p a r a m e t e r s o f l o c o m o t i o nw a s n o t c o n s i d e r e d .

I n t h e p r e s e n t i n v e s t i g a t i o n w e e v a l u a t e d t h e s ep r o b l e m s . A c c o r d i n g l y , t h e t i m e c o u r s e o f H - r e f l e x

e x c i t ab i l i t y t h r o u g h o u t t h e s t e p c y c l e w a s a n a l y z e do n t h e s o l e u s ( S o l ) m u s c l e , w h i c h w a s c h o s e n f o r i t ss i m p le m e c h a n i ca l a r r a n g e m e n t ( m o n o a r t i c u l a r ) a n df o r it s f u n c t i o n a l h o m o g e n e i t y ( s lo w m o t o r u n i ts ) .F o r t hi s p u r p o s e a n a d h o c m e t h o d w a s d e v i s e d a n dt e s t e d , a l l o w i n g a r a t h e r h i g h t i m e r e s o l u t i o n . T h ea n a l ys i s w a s e x t e n d e d t o t h r e e d i f f e r e n t p a c i n gm o v e m e n t s : b i p e d a l tr e a d m i l l w a l k i n g , s i n g l e - li m bt r e a d m i l l w a l k in g , t o o b t a i n i n f o r m a t i o n o n t h ec o n t r i b u t i o n o f c r o s s e d e f fe c t s f r o m t h e c o n t r a l a t e r a lw a l k i n g l im b , a n d s i n g l e - l i m b s te p p i n g o n o n e s p o t .T h i s l as t p a r a d i g m w a s i n c l u d e d t o a s s e s s w h e t h e r t h ee x c i t ab i l i t y c h a n g e s o b s e r v e d d u r i n g w a l k i n g w e r es p e ci fi c o f t h e a u t o m a t i c l o c o m o t o r f u n c t i o n o r w e r ec o m m o n t o o th e r v o l u n t a r y m o v e m e n t s , w h i c hi n v o l v e , a s s t e p p i n g d o e s , a s i m i l a r r h y t h m i c a c t i v a -t i o n o f f l e x o r a n d e x t e n s o r m u s c l e s .

M e t h o d s

Experimental paradigms

The experiments were carried out on eight healthy volunteers,aged between 24 and 33 years. Al l of them were tested a t leastthree t imes.

The following conditions were investigated:a) bipe dal walking on a tread mill at a stride frequency of 50

strides/min, correspon ding to a speed of appro ximate ly 4.5 km/h.After a short t ra ining per iod, subjec ts were able to walk in acom fortably erect postu re, while facing directly forwa rd andrhythmically swinging the upper l imbs, as during normal groundlocomot ion;

b) walking on treadm ill with the righ t lowe r l imb, with thecontra la tera l limb suppo rted on a f ixed adjacent pla t form. Sub-jects were asked to shift their body weight from the fixed foot tothe moving one and vice versa, as during the loading andunloading phases of the normal gait . Stride frequency was thesame as in condition a);

c) stepping on one spot with a single l imb at a frequ ency of 50strides/min. The vo lunteers were trained to prod uce a sequence offlexions and extensions of the fight lowe r l imb; the hip an d kneeangles attain ed maximal flexion values of 30-40 (thigh-pelvis) a nd120-140 (thigh-shank) degrees, respectively. The body weight wassupported by the non-performing l imb throughout the ent i re stepcycle . The rhythm was prompted by a beep tone for approximate ly1 min, and then, during the recording session, reproduced by thesubject without any acoustic cue, to avoid audio-sp inal nfluences.

In the trials involving alternate balancing of the su pport bas ebetween the fee t (paradigms a and b) , subjec ts took a 2 min restperio d after every 5 min of walking. In th e third parad igm (whichwas felt to be m ore fatiguing) 1 min of stepp ing was alternatedwith 1 min of rest .

Each exp erimen t lasted from 2.5 to 3 h and focused on one o fthe above descr ibed rhythmic movements. The protocol inc ludedmonitoring of a series of contro l variables during u nper turbed stepcycles performed a t the onset , middle and end of the recordingsession and assessment o f the excitab ili ty changes of the Sol H-reflex arc during walking or stepping.

Experimental setup and general elaboration procedures

The following control variables were monitored: kinematics oflower l imbs, relative changes in Sol length, foot-floor contactphases and EM G activity of two couples o f antagonistic muscles ofthe leg and thigh.

Low er l imb kinematics was analyze d by means of a special TVsignal processor (Elite; Ferrign o and P edot ti 1985), which alloweddetection by a TV camera (sampling rate, 50 Hz) of the instan-taneous posi t ion in space of passive re troref lec t ive markers, 3 mmin diameter, glued to the skin of the subjec t . Markers were incorrespondence with the ante rior superio r il iac crest , greatertrochanter, lateral aspect of the knee, lateral malleolus, fifthmetatarsus and heel.

A PDPll -03 minicomputer connected to the El i te processorprovided on-line the st ick diagrams of the examined m ovements,which were drawn o n a d igital plot ter (Tek tronix 4662) as straightl ines be tween the points represent ing the posi t ion of each marker.

Resolution of the system was one part in 2560 (1 mm in a squaref ie ld 2 .56 m w ide) . Data obta ined from the El i te system were a lsoemployed for the ca lcula t ion of joint angles of the hip, knee andankle. An example of the stick diagrams and time courses of thejoint angles during the thre e rhythm ic movemen ts investigated isreported in Fig. 1 . This procedure was used to obta in theindividual features of the movements under study and to checktheir reproducibili ty in the same su bject and among differentsubjects.

Changes in length of the Sol muscle during walking andstepping were also determine d. The g eom etric centroid of theproximal insertion area of the Sol muscle on the back of the t ibiaand the position of the insertion of the achilles tendon on thecalcaneum were est imated by di rec t measurements on eachSubject. The distance between these two points was taken as a


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TREADMZLL WALKING T R E A D M I L L 1 4 A L K E N G ( s i r ~ g l e l i m b ) S T E P P I N G O N O N E S P O T ( s i n g l e l l m b )

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F ig . 1 . K in em at i c an a ly s i s o f t h e t h ree rh y th m ic m o v em en t s i n v es t i g a ted . S t i ck d iag ram s in t h e u p p e r p a r t r e p resen t t h e seq u en t i ap o s i t io n s a s su m ed b y th e t e s t ed l im b d u r in g o n e cy c l e , w i th o n se t a t t h e fo o t -g ro u n d co n tac t . Tim e in t e rv a l b e tw een tw o su b seq u en t s t i cki s 2 0 m s . B lack a r ro w s a t t h e t o p m ark th e e n d o f t h e s t an ce p h ase . In t h e l o w er g rap h s , t h e t im e co u r ses o f t h e h ip , k n ee an d an k le j o inan g les (1 0 tr aces su p e r im p o sed ) a r e r ep o r t e d t o sh o w th e d eg ree o f r ep ro d u c ib i l it y w i th in o n e r eco rd in g se s s io n . H o r i zo n ta l d ash ed l i n ere fe r t o j o in t an g le s co m p u ted w h en s t an d in g u p r ig h t

m easu re o f t h e S o l l en g th an d w as co m p u ted f ro m th e an k le j o in tan g les o n th e b as i s o f a b io m ech an ica l m o d e l d esc r ib ed in d e t a i le l sew h ere (F r ig o an d P ed o t t i 1 9 7 8 ) . D a ta w ere ex p res sed a sr e l a t i v e l en g th ch an g es ( i n m m ) w i th r e sp ec t t o a co n t ro l v a lu em easu red w h i l e s t an d in g .

F o o t -g ro u n d co n tac t p h ases w ere d e t ec t ed u s in g th ree b ras sm ic ro sw i t ch es f i x ed u n d e r t h e h ee l , an d u n d e r t h e f i r s t an d th ef i f th m e ta t a r sa l h ead o f each fo o t . T h re e d i f f e r en t D C l ev e lsco r r e sp o n d ed to t h e h ee l s t r i k e , fo o t - f l a t an d fo re fo o t co n tac t .T h e y w e r e u s e d b y t h e c o m p u t e r f o r t h e m e a s u r e m e n t o f t h ed u ra t io n o f t h e s t r id e cy c le ( t im e b e tw een tw o s u b seq u e n t g ro u n ds t r ik es ) , t h e s t an ce p h ase an d i t s su b co rn p o n en t s .

E M G ac t iv i t y o f t h e S o l , t i b i a li s an t e r io r (TA ) , v as tu s l a te r a l i s(V L ) an d b i cep s f em o r i s cap u t l o n g u rn (B F ) w as d e t ec t ed b ysurface b ipo lar e lect rodes , ampl i f ied (gain 1000) and fed in to theco m p u te r ( sam p l in g f r eq u en cy 2 k H z) . P a ra l l e l o n - l i n e m o n i to r in g

was a lso p rov ided by a s to rage osci l lo scope. S ignals were d ig i ta l lyrec t i f i ed , n o rm a l i zed an d in t eg ra t ed o v e r b in s co r r e sp o n d in g to1 % o f t h e s tr i d e d u ra t io n . In each su b jec t t h e E M G p a t t e rnch a rac t e r i z in g th e d i f f e r en t p ac in g m o v em en t s w as o b t a in ed , fo rth e fo u r m u sc l e s i n v es t ig a t ed , b y av e rag in g a t l ea s t 3 0 u n p e r tu rb eds t ep cyc le s. S t an d a rd d ev ia t i o n w as a l so co m p u ted fo r eac h b in .

E M G e l ec t ro d es o n th e S o l m u sc l e a l so se rv ed to r eco rd t h eH - re f l ex . C a re w as t ak en th a t t h e i r p l acem en t w o u ld i n su rese l ec ti v e r eco rd in g o f d i r ec t (M ) an d r e f l ex r e sp o n ses f ro m th e S o lm u sc l e w i th n o co n t r ib u t io n f ro m th e g as t ro cn em iu s m u sc l e s . T h i sw as a sce r t a in ed b y ch eck in g th e w av efo rm o f t h e r eco rd edrespons es (Kotz 1973 , p 51) and the s im i lar i ty in the shape o f Man d H p o ten t i a l s (H u g o n 1 9 7 3 ) .

S o l H - re f l ex w as ev o k ed b y b ip o la r s t im u la t i o n o f t h e t i b i a ln e rv e i n t h e p o p l i t ea l fo s sa . S t im u l i w ere sq u a re - sh ap ed p u l ses

1 m s in d u ra t i o n , d e l i v e red b y a co n s t an t cu r r en t s t im u la to r (D ig i t3 T, M an g o n i ) . E l ec t ro d es w ere tw o s i l v e r cy l in de r s w i th a co n v exh em isp h e r i ca l co n tac t su r face o f 1 cm a rea , co n n ec t ed b y aP lex ig l a s b a r a t 3 cm in t e r ax i a l d i s tan ce . T h ey w ere p res s ed o n th esk in b y a p ro p e r ly sh ap ed ru b b e r p ad ( c a th o d e p ro x im a l ) an d f i x edb y an e l a st i c b an d en c i r c l in g t h e t h ig h ju s t ab o v e th e p a t e l l a . Ap ro p e r l o ca t io n w as se l ec t ed o n th e s t an d in g su b jec t i n w h ich :a ) t h e H - re f l ex co u ld b e ev o k ed w i th t h e w eak es t s t im u lu ss t r en g th , i n t h e ab sen ce o f r ad i a t i n g cu t an eo u s p a res th es i a ,b ) ch an g es i n th e d i s t an ce b e tw e en th e ca th o d e h ead an d th e t i b i a ln e rv e ( e . g . s i n k in g to a d ep th o f 5 -6 r am ) r e su l t ed i n a co -v a r i a t i o no f t h e r e f l ex an d d i r ec t r e sp o n ses acco rd in g to o n e an d th e sam erec ru i tm en t cu rv e , c ) p as s iv e f l ex io n o f t h e k n ee j o in t u p t o 4 5d eg rees d id n o t a l t e r t h e sh ap e o f t h e M w av e r ec ru i tm en t cu rv e ,w h i l e d isp l acin g th e w h o le cu rv e t o w ard th e r i g h t s i d e. T h e ab o v ec r i t e ri a w ere m e t i n 8 su b jec t s ch o sen fo r t h e s tu d y o u t o f 1 5

can d id a t e s sc reen ed .

H-reflex measurement under dynamic conditions

T h e u se o f t h e H - re f l ex m e th o d fo r t h e a s ses sm en t o f t h eex c i tab i li t y o f t h e S o l m y o ta t i c a r c i s b ased o n th e co n cep t t h a t i nth e p resen ce o f co n s t an t s t im u la t i o n o f I a f i b e r s , an y ch an g e inref lex response is the consequence o f exci tab i l i ty f luctuat ionso ccu r r in g in t h e sp in a l co rd (m o to n eu ro n es an d /o r p re sy n ap t i cin h ib i t io n o f I a t e rm in a l s ) . D u r in g w a lk in g an d s t ep p in g , ch an g esin s t im u lu s e ff ect i v en ess , m a in ly d u e t o i n ad v e r t en t m o v e m en t s o fp o p l i t ea l e l ec t ro d es w i th r e sp ec t t o t h e t i b i a l n e rv e , can n o t b eav o id ed . T h ese o ccu r d esp i t e co n s t an t cu r r en t d e l i v e r in g an d ,


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H-response ampl i~ude

F ig . 2 . A Ty p ica l r e f e ren ce cu rv e r eco rd ed in co n t ro l s t an d in gposi t ion . Orig inal data po in ts are f i t ted by an 8 th degree po lyno-m ia l cu rv e o b t a in ed b y th e l eas t sq u a re m e th o d . B E x am p le o fm eas u rem en t o f t h e ex c i tab i l it y lev e l u n d e r d y n am ic co n d i t i o n s .F i l led d i am o n d r ep re sen t s t h e am p l i t u d e o f t h e H - re f l ex o b t a in edb y a s t im u lu s , d e l iv e red d u r in g th e seco n d h a l f o f th e s t an ce p h ase(38% of the s tep cycle) . The abscissa o f the same po in t i s theam p l i t u d e o f th e a s so c i a t ed M w av e . A H i s t h e d i f f e r en ce b e tw eenth e am p l i t u d e o f t h e ab o v e H - re f l ex an d th e am p l i t u d e ex p ec t edfo r t h e sam e M resp o n se o n th e r e f e ren ce cu rv e r eco rd ed a t r e st .T h i s v a lu e , ex p res sed in m V, w as co n s id e red a s a m eas u re o f t h eexci tab i l i ty s ta te a t the ins tan t o f s t imulus del iver ing . A c lear-cu tfacih ta t ion is ev ide n t in th is case . Th e two ver t ical dashed l inesin d i ca te t h e r an g e o f v a r i ab il i ty o f t h e M resp o n se accep ted fo r t h eab o v e m ea su rem en t ( see t ex t ) . I n t h i s case , i t li e s b e tw ee n 4 an d2 5 % o f M m ax . T w o s t an d a rd e r ro r s a r e a l so i n d ica t ed w i th in t h i sw o rk in g r an g e b y th e h a t ch ed a reas

p ro v id ed s t im u l i ab o v e th e t h re sh o ld fo r t h e m o to r f i b e r s a r eap p l ied , can b e r e f l ec ted b y ch an g es i n t h e s i ze o f t h e M w av e . Toal low the exci tab i l i ty o f the H-ref lex arc to be assessed un derd y n am ic co n d i t i o n s , n o tw i th s t an d in g th e ab o v e ch an g es i ns t imulus effect iveness , the fo l lowing p rocedure was dev ised andtes ted .

In t h e f i r s t p a r t o f t h e ex p e r im en t , a r e f e ren ce ex c i tab i l it yl ev e l w as d e f in ed fo r t h e su b jec t u n d e r s tu d y, w h o m a in t a in e d as t an d in g p o s tu re , w i th t h e b o d y w e ig h t eq u a l ly su p p o r t ed b y th etw o lo w er lim b s . A cco rd in g ly, r ec ru i tm en t cu rv es o f t h e H an d M

resp o n ses w ere o b t a in ed b y p ro g res s iv e ly i n c reas in g th e s t im u lu ss t r en g th . T h e am p l i t u d e o f each H - re f l ex w as t h en p lo t t ed ag a in s tt h e s i ze of t h e a s so c i a t ed M w av e , an d th e ex p e r im en ta l v a lu esf i t t ed b y a p o ly n o m ia l fu n c t io n ( l eas t sq u a re m e th o d ) . S u ch acu rv e , w h ich w as o b t a in ed ag a in a t t h e en d o f t h e se s s io n to ch eckth e s t ab i li t y o f t h e ex p e r im en ta l co n d i t io n s , w as s to red in t h eco m p u te r a s t h e r e f e ren ce ex c i t ab i li t y l ev e l (F ig . 2 A ) . M ax im u mH-ref lex s ize in th is con tro l s i tuat ion was 47 + 14% (SD n . 24cu rv es ) o f t h e m ax im a l M w av e (M m ax ) .

In t h e su b seq u en t p a r t o f t h e se s s ion , s t im u lu s i n t en s it y w asse t t o ev o k e H - re f l ex es a s so c i a t ed w i th sm a l l M w av es (1 0 -1 5 % Mm ax ) . S u b jec ts s t a r t ed w a lk in g an d , p ro v id ed s t ead y s t a t e co n d i -t i o n s w ere ach i ev ed ( i . e. , w h en s t r i d e d u ra t i o n d id n o t ex ceed p lu so r m in u s 1 0 % o f t h e p re f ix ed v a lu e ) , an i n t e r ac t i v e co m p u te rp ro g ram in i t i a t ed s t im u lu s d e l iv e ry. A p p ro x im a te ly 1 0 0 s t im u l iw ere ap p l i ed r an d o m ly in d i f f e r en t p h ases o f t h e s t r i d e (o n e ev e ry5 -1 0 cy c l e s ) , an d th e ev o k ed M an d H - resp o n ses w ere m easu redo n - l i n e . D u r in g p ac in g , t h e am p l i t u d e o f t h e M w av e co u ldincrease o r decrease wi th respect to the value selected a t res t ( i . e .1 0 -1 5 % o f M m ax ) , a t t a in in g ex t r em e v a lu es o f 1 t o 3 5 % M m ax .T h i s v a r iab i l it y w as m o s t o f t en u n p red i c t ab l e an d n o co m m o nt ren d co u ld b e fo u n d am o n g th e v a r io u s su b jec t s ex am in ed . F o r

each M -w av e th e ex p ec t ed am p l i t u d e o f t h e a s so c i a t ed H - re f l exw as au to m at i ca l ly se l ec t ed i n t h e r e f e ren ce cu rv e r eco rd ed a t r e s t ,an d th e d i f f e r en ce b e tw een ac tu a l an d ex p ec t ed H - re f l ex , ex p re -s sed in m V (A H ) , w as t ak en a s a m easu re o f t h e r e l a t iv einstan tan eous exci tab i l i ty level (see F ig . 2B ) .

To ru l e o u t p o ss ib l e co n fo u n d in g s , t h e v a r i ab i l it y o f t h e Mw av e s i ze w as l im i t ed t o a w in d o w se l ec t ed i n t h e r e f e ren ce cu rv ein w h ich M -resp o n ses w ere a s so c i a t ed w i th n ea r m ax im a l H -re f l ex es . In o u r su b jec t s t h i s w in d o w u su a l ly sp an n ed b e tw een 4an d 2 5 % o f t h e m ax im a l M w av e ( see v e r ti ca l d ash ed l i n es i n th eex am p le o f F ig . 2 B ) . T h e r easo n s fo r t h i s r e s t r ic t i o n a r e t h efo l lo w in g . A t t h e l o w es t M w av e am p l i t u d es , sm a l l ch an g es o f af ew h u n d red m ic ro v o lt s i n M resp o n se w ere fo u n d to b e a s so c i a tedw i th u p to t en - fo ld ch an g es i n H - re f l ex am p l i t u d e (1 -2 m V ) . T h ee r ro r i n d e t e rm in in g th e "ex p ec t ed " H am p l i t u d e fo r t h ese n ea r-

th re sh o ld M w av es w o u ld t h e re fo re h av e b een to o l a rg e . O n th eo th e r h an d , M w av es ex ceed in g th e u p p e r l im i t ch o sen w ereassociated wi th H-ref lexes ly ing def in i te ly in the fa l l ing s lope o fth e i r r ec ru i tm en t cu rv e , w i th co n seq u en t sh o r t co m in g s d u e to t h eh eav y an t id ro m ic ac t i v a t io n o f t h e m o to r f i b e r s .

T h e p o ss ib i li t y t h a t ev en w i th in su ch a w o rk in g r an g e , t h ed ifferen t sensi t iv i ty o f the tes t H-ref lex to faci l i ta t ion o r inh ib i t ionmigh t b ias the es t imated exci tab i l i ty changes (see Meinck 1980)seems very un l ikely, a t leas t fo r the effects under s tudy. In fact , aco n t ro l ex p e r im en t h as sh o w n th a t"pre-maximal"est H-ref lexes(a t t h e l e f tm o s t en d o f t h e w o rk in g r an g e ) , a s w e l l a s "p o s t -m ax im a l " o n es ( a t t h e r i g h tm o s t en d ) d i sp l ay ed co m p arab lech an g es i n am p l i t u d e , w h en ev o k ed in a s am e p h ase o f t h e s t epcyc le ( i n c rease u p to 4 m V b e tw een 3 5 an d 4 2 % , an d d ec reaseb e tw een 6 0 an d 7 0 % ) . M o reo v e r, d esp i t e t h e co m p le t e ly d i f fe r en t

d i s t r i b u t io n o f t h e t e s t H - re f l ex am p l i t u d es t h ro u g h o u t t h e s t epcycle , as judged by analysis o f the ampl i tudes o f the evoked Mw av es , a l l t h e su b jec t s ex h ib i t ed a s im i l a r p a t t e rn an d t im e co u r seo f t h e H - re f l ex m o d u la t i o n .

P re l im in a ry co n t ro l t e s t s w ere a l so ca r r i ed o u t t o a sce r t a inw h e th e r, w i th in t h e l im i t s o f o u r ex p e r im en ta l co n d i t i o n s , t h eam p l i t u d e o f t h e M resp o n se co u ld b e u sed a s a m easu re o fs t imulus effect iveness . In fact , possib le b ias ing facto rs cou ld ar isef r o m t h e E M G b a c k g r o u n d ( s u m m a t i o n o f t he t w o s i g n al s u n d e rth e r eco rd in g e l ec t ro d es o r o cc lu s io n b e tw een ex t e rn a l s t im u lu san d e ff e r en t t r a f fi c i n t h e m o to r f i b e r s) an d f ro m s i zab le ch an g es i nS o l l en g th (v o lu m e co n d u c to r p a ram e te r s ) . A s sh o w n in F ig . 3 , i tw as fo u n d th a t , ev en in t h e p resen ce o f v o lu n ta ry E M G ac t iv i ty a sh ig h a s 3 0 % o f t h e m ax im u m i so m et r i c lev e l ( co r r e sp o n d in g to t h em ax im a l v a lu e a t t a in ed d u r in g w a lk in g an d s t ep p in g ) t h e


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M H M H

1

A b d -

Hal I .

2 0 m s ] 1 m V

Fig . 3 . Effect o f increasing background EMG act iv i ty on therecorded M w ave f rom the So l muscle . The lef t co lumn refers to asmal l M wave (4% M max) , the r igh t to a larger one (16% Mmax) . From top to bo t tom , con t ro l responses a t res t and effects o fvo lun tary ton ic con t ract ions o f the So l muscle o f increasingst reng th (15 to 60% of the maximal EM G ampl i tude) are repor ted .In each pai r o f traces , the upp er i s f rom the So l and the lower f romthe abductor hal lucis (Abd Hal l ) , which i s a l so suppl ied by thet ib ial nerve bu t s i len t dur ing So l con t ract ion ; the M wave on theAbd Hal l was used to moni to r the constancy of the s t imulusappl ied to the t ib ial nerve. I t appears that increasing EM Gbackground does no t in f luence the am pl i tude and the shape o f thetwo d i fferen t M w aves f rom Sol muscle up to 30% o f the maximumEM G level , corresponding to the l imi t value at ta ined in the moto rtasks invest igated in the p resen t s tudy. An obvious in ter ferencewi th the recorded response i s ins tead p resen t fo r h igher EM Glevels (45 and 60% of maximum). Note the wel l -known behav iorof the H-ref lexes , which increase thei r ampl i tude along wi th theE M G ac t i v i t y

ampl i tude and shape o f a g iven M w ave ( f rom 5 to 20% of M max)were no t modif ied . These resu l t s were conf i rmed in a range o fank le jo in t ang les between +15 and -15 degrees . The largerampl i tude o f the M waves adopted com pared to the locomoto rE M G b ack g ro u n d , t h e ab sen ce o f o v e r l ap p i n g b e t ween mo t o rf ibers act ivated by the cen t ral command (smal l s ize) and by theex ternal s t imulus ( larger s ize), and the sm al l changes in S o l leng thoccurr ing in the m otor tasks invest igated migh t exp lain the lack o fin ter ference o f the above po ten t ia l ly b ias ing facto rs in ourexper imental condi t ions .

5 3

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Fig . 4 . Comparat ive analysis o f the t ime course o f So l H-ref lexexcitabil i ty during bipedal treadmill walking at 50 strides/min. Inthe upper g raph changes in ref lex exci tab i l ity are expressed in mV(posi t ive and negat ive values) , wi th respect to a reference level(+ 2 SE) ob tained in a s tand ing posi t ion . Such a value ( l ine 0 )corresponds to con t ro l H-ref lexes c lose to H max (5 mV in th iscase) , bu t no t necessar i ly constan t in ampl i tude (see Methods) .Stride onset is at the heel-strike instant. Stance-swing transit ion ismarked by the ver t ical dashed l ine. So l leng th changes arerepor ted in the second graph (10 t races super imposed) . Relat iveleng th changes are represen ted wi th respect to a reference valuecomputed in s tand ing posi t ion . Average EMG act iv i ty, rect i f iedand mediated over b ins corresponding to 1% of the s t r ide (+ SD)is reported for soleus (Sol), t ibialis anterior (TA), vastus lateralis(VAL) and b iceps femoris (BF) . Foo tground con tact phases arealso represen ted in the d iagram at the bo t tom by th ree d i fferen tlevels corresponding in sequence to the heel -s t r ike, foo t - f la t andforefoo t con tact

R e s u l t s

Excitability of Sol H-reflex during bipedal treadmillwalking

F i g u r e 4 r e p o r t s a n i l l u s tr a t i v e e x a m p l e o f t h e t i m e

c o u r s e o f t h e e x c i t a b i l i t y o f t h e S o l H - r e f l e x d u r i n gb i p e d a l t r e a d m i l l w a l k i n g , a l o n g w i t h S o l l e n g t hc h a n g e s, E M G s a n d f o o t - g r o u n d c o n t a c t p h a s e s .M o d u l a t i o n s a r e e x p re s s e d i n m V ( p o s i t i v e a n dn e g a t i v e v a l u e s ) w i t h r e f e r e n c e t o t h e c o n t r o l l e v e ld e t e r m i n e d i n a st a n d i n g p o s i t i o n . I t c a n b e s e e n t h a t


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5 4

T R E A D N I L L W A L K I N G ( s i ~o l e l i m b )

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i

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',I - t - I

e IOO gpercen loge o s l ~ e cy c I e

Fig. 5. Comparative analysis of the time course of Sol H -reflexexcitability during treadm ill walking perform ed by a single limb,with the contralateral suppo rted by a fixed platform. The sub ject sdifferent than tha t of the preceeding figure. Graphs have the samesignificance as in Fig. 4

a t t he ins t an t o f t he hee l - s t r ike , t he exc i t ab i li t y o f t heH- re f l ex i s s ign i f i can t ly r educed compared to there f e r ence cond i t ions . Th i s phenomenon occur s a t amusc le l eng th c lose to the con t ro l va lue , and i sconcur r en t wi th s imul t aneous ac t iva t ion o f the fourmusc les t e s t ed . EM G ac t iv ity from ca l f musc les in theear ly s tance , w h ich is unusua l dur ing f loor, bu t qu i t ecommon dur ing t r eadmi l l wa lk ing ( see Mur ray e t a l .1985) , was r ecorded in 7 ou t o f 8 sub jec t s t e s t ed .Wi th in the f i r s t 10% of the s t r ide , t h i s l ocom otorE M G w a s r a t h e r c o n s t a n t i n a m p l i t u d e o r p r o g r e s -sively increa sed, b eing al to geth er s ignif icant ly highercompared wi th the t i ny ac t iv i ty (mos t o f t en a f ewmotor un i t s ) obse rved in the r e f e r ence s t and ingpos tu re .

A s t h e f o r e f o o t so l e a p p r o a c h e s t h e g r o u n d , S o ll eng th i s s li gh tly decrease d o r s t ays cons tan t , due tot h e c o n t e m p o r a n e o u s f o r w a r d d i s p l a c e m e n t o f t h eshank (see length t races in the f igure) . In th is phasethe H - re f l ex exc i tab i l i ty r ega ins i t s re f e r enc e r ange tob e s li gh tl y e n h a n c e d b e t w e e n 1 0 a n d 2 0 % o f th e s t e pcyc le in r e l a tion to the r i se in So l EM G ac t iv ity andSol s t re t ch ing . Subs equen t ly, a f t e r a shor t r ecoveryto the con t ro l l eve l , a t abou t 20% of the cyc le , a

marked inc rease in r e f l ex exc i t ab i l i t y t akes p l ace ,dur ing the quas i - i somet r i c con t r ac t ion o f So l musc le .Th i s f ac i li t a to ry e f f ec t c lose ly r ep li ca t es the enve lo peo f t h e S o l E M G a n d p e a k s i n th e s e c o n d h a l f o f t h es t ance , i n phase wi th the max imum So l ac t iva t ion .

In pa ra ll e l wi th the de rec ru i tm en t o f So l mo to run i t s , t he H- re f l ex ampl i tude undergoes a markeddecrease , w h ich las t s t he en t i r e swing phase . Such aneff ec t i s max imal a round the toe -o f f pe r iod , wh en theSo l musc le i s c lose to i t s max imum shor t en ing , and inthe l a s t swing phase . Ho w eve r, i t i s l e ss p ronoun cedb e t w e e n 7 0 a n d 8 0 % o f t h e c y c l e , w h e n t h e m e c h a n i -ca l e f f ec t o f TA ac t iva t ion s t r e t ches the So l towa rd i t sr e f e r ence l eng th .

The desc r ibed p ic tu re was r ep roduc ib le in a l l t hesub jec t s exam ined , a s r egards the sequ ence o f theexc i t ab il i ty changes and the i r phase r e l a t ionsh ip wi thSo l l eng th and EM G ac t iv ity. Ho w eve r, a r a the r h igh

var i ab i l i t y was observed in the in t ens i ty o f t hed i ff e re n t p h e n o m e n a . T h e i n te n s i ty w a s d e t e r m i n e din each sub jec t by normal i z ing the max imalampl i tude o f the main f ac i l it a to ry and inh ib i to ryef f ec t s (mean va lue o f the 5 ex t r em e da ta po in t s ) t othe s ize o f the max imal M -wa ve (M max) . T h i sp e r c e n t v a l u e p r o v i d e s a m e a s u r e o f th e p r o p o r t i o no f th e S o l m o t o n e u r o n p o p u l a t i o n , q u a n t i fi e d a s awho le by M max , invo lved in any one e f f ec t .

O f the e igh t sub jec t s t e s t ed , t he decrease in theexc i tab i l it y o f t he So l H- re f l ex ob served a t hee l s t r ikecovered , a t it s max imal in t ens i ty, 27 + 14% (mea n _+

S D ) o f M m a x . T h e p e a k a m p l i tu d e o f t h e l a rg e e n d -stance faci l i ta t ion involv ed 35 +_ 11% (m ean __ SD )of the max imal m oto r r esponse . I t s t e rmina t ion in a l lsub jec t s c lose ly pa ra l l e l ed the end o f So l EM Gact iv i ty, wh ich r anged f rom 42 to 50% of the s t epcycle . The long- last ing decrease in exci tabi l i ty thatcharac te r i zed the swing phase a t t a ined i t s peak l eve la t abou t 60% of the cyc le , wi th an ampl i tudecor r espond ing to 46 _+ 8% of M m ax (m ean + SD) .S ince the max imal H- re f l ex in the con t ro l s t and ingpostu re wa s 47 _+ 14% (me an _+ SD ) of M ma x, i ta p p e a r s t h a t e v e n n e a r m a x i m a l H - r e s p o n s e s c o u l dbe com ple te ly inh ib i t ed in th is phase o f the s t ride . A t70 to 80% of the cyc le , du r ing the abov e desc r ibeda t t enua t ion o f the swing-phase inh ib it ion , m ax imalin t ensi ty o f i nh ib it ion was 17 _ 10% (mea n _ SD ) o fM m a x .

Excitability of the Sol H-reflex during single-limbtreadmill walking

In b ipeda l and s ing le - l imb t r eadmi l l wa lk ing ,k inemat i cs o f t he moving l imb were subs tan t i a l lys imi la r ( see F ig . 1 ). Ho we ver, t he E M G pa t t e rn


7/12

u n d e r l y i n g t h e l a t t e r m o t o r t a s k w a s f o u n d t o b equ i t e spec i f i c . Record ings in F ig . 5 c l ea r ly show thescarce ly modu la t ed ac t iv ity o f t he So l musc le ( ab -sence o f a c l ea r push-o ff bur s t ) , t he anom alousp r e s e n c e o f TA a c t iv i ty d u ri n g t h e w h o l e s t a n c e

p h a s e , t h e l a c k o f c on s i s te n t E M G i n V L , a n d t h ea l m o s t c o n t i n u o u s l o w l e v e l c o n tr a c t io n o f B F.H- re f l ex t es t ing dur ing s ing le - l imb t r eadmi l l

wa lk ing r evea led the pe r s i s t ence o f the m ain e f f ec t so b s e r v e d d u r i n g b i p e d a l w a l k i n g , n a m e l y a d e c r e a s ein exc i t ab i li t y a t t he hee l s t r ike , f o l lowe d by a r e l a t ivefac i l i t a t ion , max imal in the l a t e s t ance , and aga in byan inh ib i t ion dur ing the sw ing phase ( see F ig . 5 ). Arecovery toward the con t ro l exc i t ab i l i t y l eve l wasf o u n d i n t h e m i d s t a n c e , b u t n o d e c r e a s e i n t h einh ib i tion w as p resen t i n mid swing . Th i s pa t t e rn w ascons i s t en t ly observed in the 8 sub jec t s i nves t iga ted .N o s ign if i can t changes in max imal in t ens i ty o f t hes t ance phase f ac i li t a t ion (30 +_ 13% M max , me an +SD ) o r the swing phase inh ib i t ion (41 + 12% M max ,m e a n _+ S D ) c o m p a r e d t o b i p e d a l w a l k in g w e r es h o w n . H o w e v e r, a l o w e r a m p l i t u d e o f t h e h e e l -s t r ike inh ib i t ion was obs erve d (12 + 6% M m ax ,m ea n +_ SD ) .

Excitabil i ty of Sol H-reflex during steppingo n o n e s p o t

I n t h i s n e w s e q u e n t i a l m o v e m e n t , f o o t - g r o u n d c o n -

t a c t w a s m a d e o n t h e f o r e f o o t a n d n o t o n t h e h e e l , a sdur ing t r eadmi l l wa lk ing . The ea r ly s t ance phase wascharac te r i zed by a s t r e tch ing o f the So l musc le whichlas t ed ab ou t 20 % of the s t ep cyc le (180 to 220 ms) ,fo r a ca l cu la t ed l eng th -change o f 1 to 1 .3 cm ( seeF i g . 6 ). A c o n s p i c u o u s E M G b u r s t w a s r e c o r d e df rom So l , s t a r t ing approx imate ly 200 ms befo re andp e a k i n g a r o u n d t h e f o o t - g r o u n d c o n t a c t i n st a n t. S u c ha l eng then ing con t r ac t ion (So l "y ie ld ing" ) has adum ping e f f ec t on the land ing phase . I n the ea r lys t a n c e , t h e S o l H - r e f l e x a m p l i t u d e w a s f o u n d t o b ewi th in the r e f e r ence r ange in seven sub jec t s ands ign i f i can t ly lower in one , i n whom the max imalinh ib i to ry e f f ec t i nvo lved 12% of the m ax imal Mr e s p o n s e .

D u r i n g t h e m i d - s t a n c e t h e f o r e f o o t s o l e h a d t h ela rges t con tac t a r ea wi th the f loor, bu t t he hee l wass ti ll kep t s l igh t ly r a i sed , w e igh t su ppor t be ing e n t i r e lyaccom pl i shed by the con t r a l a t e r a l l ow er l imb . TheS o l l e n g th r e a c h e d a p l a te a u l e v e l , w h e r e a s S o l E M Gdisp layed low amp l i tude sus t a ined ac t iv ity (2 sub-j ec t s ) , w as segm ented in d i sc r e t e bur s t s (3 sub-j ec t s ) , o r was absen t (3 sub jec t s ) . The t ib i a l i san te r io r w as to t a l ly s i len t o r, a s show n in the ex am pleof F ig . 6 , w as ac t iva ted in r e l a t ion to the s i l en t pe r iod

55

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2 4.

o.

~ o

_ z

sO"

SO L

TA

VA L

S T E P P I N G O N O N E S P O T ( ~ im g l e l im b }

E m V 3 M m a x = I g . 6 m V

H m o x = 4 . 2 m V

. . . . . . . . . " . - i" o - . . . . . . . . . ..: ] . , - ' . " ".

[ ~ r n ] I

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p e r c e n t a g e o f k h e c y c l e

F ig . 6 . C o m p ara t iv e an a ly s i s o f t h e t im e co u r se o f S o l H - re f l exexci tab i l i ty dur ing s ing le l imb s tepp ing o n on e spo t a t 50 paces/m in . T h e v a r i ab l e s an a ly zed a re t h e sam e as i n F ig s . 4 an d 5

on the an tagon i s t ic So l musc le . I r r espec t ive o f the

a b o v e d e s c r i b e d v a r ia b i li ty i n th e E M G p a t t e r n , t h eexc i t ab i l i t y o f t he So l H- re f l ex was s ign i f i can t lylow ered in a ll cases be tw een 15 and 30% of the s t epcyc le , wi th a pe ak amp l i tude o f the e f f ec t i nvo lv ing10 _+ 7% (m ean _+ SD , 8 subjec ts) of M m ax. I t i sn o t e w o r t h y t h a t t h i s t i m e w i n d o w w a s t h e s a m edur ing which , i n b ipeda l and s ing le l imb t r eadmi l lwa lk ing , t he s t ance phase f ac i l i ta t ion was in t e r rup tedby a r ecove ry to o r t owa rd the r e f e r en ce exc i t ab i l i tylevel .

T h e l a te s t a n c e p h a s e o f t h e s t e p p in g m o v e m e n tw a s m a r k e d b y a c o n s i s te n t b u r s t fr o m t h e S o l m u s c l e(be tw een 30 and 55% of the cyc le ) which under l i e st h e p u s h i n g u p o f t h e h e e l . T h e S o l H - r e f l e x b e h a v e din th is phase as dur ing the walking task, exhibi t ing adist inct faci l i ta t ion which involved 24 _+ 14% (mean_+ SD , 8 sub jec t s ) o f the M response . Aga in , a ss h o w n i n t h e w a l k i n g m o v e m e n t s , i t u n d e r w e n t am a r k e d i n h i b i t i o n t h r o u g h o u t t h e s u b s e q u e n t s w i n gphase wi th a max imal va lue o f 30 _+ 8% of M max(me an _+ SD , 8 sub jec t s ) a round the toe o f f i n s t an t.In the l a s t swing phase , i n r e l a t ion to the ea r lyac t iva t ion o f the So l musc le , t he exc i t ab i li t y o f t heS o l H - r e f le x r e c o v e r e d t o w a r d s t h e r e f e r e n c e l e v e l ina l l t he sub jec t s examined .


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D i s c u s s i o n

In t h e t h r e e p a c in g mo v e me n t s e x a min e d in o u rs tudy, the exc i tab il ity o f the So l H-re f lex a rc u nder-went phase-dependen t modula t ions . A f i r s t genera l

observation is that , despite conspicuous differencesin k inemat ics , dynamics and degree o f au tomat ismb e tw e e n th e t h r e e mo to r p e r fo rma n c e s , a c o mmo nexcitabili ty patte rn w as actually identif ied. This con -sis ted of a faci l i ta t ion, maximal in the second half ofthe s tance phase, and a long last ing inhibit ion whichoccurred dur ing the la te s tance and a lmos t the wholeswing phase . Such a s te reo typed pa t te rn was a lsore ta ined when pac ing was per formed by a s ing lel imb. Since maximal ampli tudes of faci l i ta tory andinhibitory effects involved similar proport io ns of theSol motoneuron poo l in b ipeda l and s ing le l imbwalk ing , c rossed e ffec ts f rom the con t ra la te ra l mov-ing l imb do no t appear to be re levan t in subserv ingth is main mo dula t ion pa t te rn .

In the fo llowing paragraphs the poss ib le ne ura lmechan isms under ly ing the ea r ly s tance modu la t ions ,s tance phase facil i ta t ion a nd swing phase inhibit ionare d iscussed separa te ly. T he main l ine o f reason ingwas a com par ison be twe en the exc i tab i li ty o f the So lmotoneurons (MNs) as assessed by the H-re f lexmethod and the one expec ted on the bas is o f So lEMG ac t iv i ty and re la t ive musc le leng th ( see Got t -lieb et al. 1970).

Ear l y s tan ce mo d u l a t i o n s

During treadmill walking, a t the heel s tr ike instant ,the ank le jo in t ang le and the ca l f musc le leng th a reclose to their control value and, in most cases, anEM G ac t iv i ty h igher than du r ing s tand ing , andprogress ive ly increas ing , i s recorded f rom the So lmuscle (see Results and Fig. 4 , 5) . An even largerEM G discharge is p roduced in the ea r ly s tance phaseof the s tepping task (Fig. 6) .

On the ev idence o f H-re f lex s tud ies per fo rmedunder s ta t ic condit ions, the described si tuationswould predict a r ise in the excitabil i ty of the Sol H-re f lex , compared wi th the con t ro l leve l . In fac t ,a ) the exc i tabi l ity o f a vo lun ta ry ac t iva ted M N poolincreases a long wi th the ton ic EMG leve l (Pa i l la rd1955; Kotz 1977; Gott l ieb and Agarwal 1973; Kear-ney and Hu nte r 1983; Sch ieppa t i and C renna 1984 ,see also the example in our Fig. 3); b) in the earlydynam ic phase o f mo tor un i t rec ru i tm ent (as in thecase o f So l musc le near the beg inn ing of the s tancephase) , the exc i tab i l i ty o f the ac t ive motor nuc leusma y b e e v e n h ig h e r th a n d u r in g c o r r e s p o n d e n t t o n i ccontractions (Gott l ieb et a l . 1970); c)reciprocal

inh ib ito ry e ffec ts f rom the an tagonis t musc le ( the T Ain the p resen t case ) were shown to be depressedduring activation of the agonist (Sol) MN pool ( l ies1986).

Unexpec ted ly, in con t ras t w i th the above

not ions , we found tha t , in the f i r s t 10% of the s tepcycle , the Sol H -reflex was not fa ci l i ta ted; instead, i twas cons is ten t ly inh ib i ted (12 to 27% of the MNpool) during treadmill walking, and clearlyu n c h a n g e d c o m p a re d to t h e r e f e r e n c e le v e l d ur ingstepping on the spot . In view o f the relat ively lowactivi ty level of the Sol muscle , an occlusionphenomenon i s qu i te un l ike ly. Moreover, we haveshown tha t H-re f lexes o f d i ffe ren t ampl i tude ,s u p e r imp o s e d o n a v o lu n ta ry E M G b a c k g ro u n d , ma ybe fac i l ita ted wi thou t sa tu ra t ion up to E M G leve lscons iderab ly h igher than those ob served dur ing walk-ing and stepping (Fig. 3) . R ath er, two diffe rentin te rpre ta t ions m igh t be env isaged .

First , one should assume that , in spite of asupra th resho ld (EM G) ac t iv i ty m ore in tense thanduring standing, a s ignif icantly low er fraction o f theSol MNs should be d ischarged by the re f lexogen icvo l ley in the ea r ly s tance phase , du e to an increasedpostsynaptic inhibition acting on th e s i lent MN s. Th ishypothes is would im ply a to ta l ly d i ffe ren t behav iourof the exc i tab i l i ty o f a same motor nuc leus , whenrecru i ted in s ta tic and dynam ic condi tions .

Al te rna t ive ly, the d isc repancy be tween ac tua land expec ted exc i tab i li ty leve l migh t be in te rpre ted

in te rms of p resynap t ic ga t ing o f Ia inpu t , whichwould leave So l MNs f ree to be f i red by thelocomotor command, whi le reduc ing the e ffec t ive-ness o f au togene t ic exc i ta t ion . Indeed , severa l an i -mal s tud ies have show n tha t a cen t ra l con t ro l o f thepr imary (and Ia ) a ffe ren ts is invo lved in the mo dula -t ion o f re f lex t ransmission dur ing ga i t (S hom burg an dBehre ns 1978; Bayev 1978; Bay ev and K os tyuk 1982;Dubuc e t a l . 1985) . Fur thermore , o ther re f lexo log icinves t iga t ions per fo rmed in man dur ing walk ing , bymea ns o f d iffe ren t exper im enta l approaches , po in t tothe p resence o f a p resynap t ic inh ib it ion o f Ia te rmi-nals in the early s tance phase. M orin et a l . (1982), ina s tudy on the exc i tab i li ty o f the H-re f lex , te s ted a tthe very onse t o f So l EMG ac t iv i ty dur ing g roundwalk ing , repo r ted a lower exc i tab i li ty leve l compa redwi th the same con t rac t ion reproduced vo lun ta r i ly.S ince the So l locom otor du ty cyc le s ta r t s be tw een 10and 20% of the s t r ide (P las e t a l . 1959; Basm aj ian1967), the inhibitory effect described by theseau thors seems s l igh t ly de layed wi th respec t to thepresen t resu l t s (0 -10%). D iffe rences in the rec ru i t -me n t t ime o f S o l mu s c l e b e tw e e n g ro u n d a n d t r e a d -mill walking (see Murray et a l . 1985) might accountfor the abo ve mi ld d i ffe rences in re f lex modula t ion .


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Again , p resyn ap t ic b lock ing of g roup I a ffe ren ts wassugges ted as a poss ib le m echan ism acco unt ing fo r thecomple te ga t ing o f the shor t la tency (mono-o l igo-synap tic ) comp onen t o f the So l s t re tch re f lex , te s tedby impos ing br isk acce le ra t ions to the moving t read-

mill , during theear ly s tance of na tu ra l speed w alk ing(from 0 to 10% acco rding to Figs. 3 to 6 and results inBe rger et a l . 1984, and 40 ms after the h eel s tr ike inDietz et a l. 1985). Finally, the a bsenc e of the sho rtla tency s t re tch re f lex on ca l f musc les has beendescr ibed in man a t the f loor-con tac t phase o f o therpac ing movements , such as b ipeda l hopping anddownward s tepp ing (Melv i l l Johnes and Wat t 1971;Conra d e t al . 1985) . Hen ce , m ovem ents imply ingb o th h e e l a n d fo r e fo o t g ro u n d c o n ta c t s e e m to b eassoc ia ted wi th s imi la r inh ib ito ry phen om ena .

A poss ib le func t iona l ro le o f ga t ing the m yota t icre f lex in the ea r ly s tance phase migh t be to coun-te rac t the au togene t ic exc i ta t ion f rom t r iceps surae ,which is s tretched during this s tr ide period. In thisregard i t is noteworthy that in spast ic i ty, in which alowered e ff ic iency of p resynap t ic inh ib i t ion i s wel ldocu me nted (e .g . De lwaide 1973; P ie r ro t -Dese i l -l igny and M azie res 1985; Cren na and Fr igo 1985b),the g round-con tac t phase o f ga i t i s f requen t ly h in -dered by ea r ly c lon ic act iv ity on ca l f musc les (Con radet a l. 1983; Kn utsson 1985; Cr en na a nd Frigo 1985a),which migh t be due to unga t ing o f the incoming Iadischarge.

H o w e v e r, e x p e r ime n ta l e v id e n c e in n o rm a l s u b -

jec ts sugges ts tha t au togene t ic exc i ta t ion f rom ca l fmusc les , s t re tched dur ing the con tac t phase , i s no talways ineffective. Instead, i t can be exploited toenhance the p ropuls ive phase in those pac ing move-ments in which , due to the ra the r h igh speed , y ie ld ingand push o ff a re merged in a s ing le musc le con t rac -t ion . Actua l ly, in such motor per fo rmances , fo rexample f ree runn ing , and runn ing or jumping inp lace a t a p re fe r re d f requency , a func t iona l con t r ibu-t ion o f the s t re tch re f lex has been demons t ra ted(G re e n w o o d a n d H o p k in s 1 9 7 6 ; D ie t z a n d N o th1978; Dietz et a l. 1979). A certa in " task dep end en ce "in the ea r ly s tance mod ula t ion o f the So l myota t ic a rcis the re fo re conce ivab le .

S t ance p has e f ac i l i t a ti on

In the second ha l f o f the s tance phase , So l MNs f i reat their maximal level in the s tep cycle . Thus, anincrease in the exc i tab i l i ty o f the re la t ive H-re f lexa rc, p e a k in g in c o n c u r r e n c e w i th t h e m a x imu m E M Gactivity, is expected. Interest ingly, recent s tudiesp e r fo rme d in t h e c a t h a v e s h o w n a n in c r e a s e d g a in o fthe So l H-re f lex dur ing the ex tens ion (s tance) phase

of t readmil l wa lk ing (Ak azaw a e t a l . 1982; Tay lor e tal. 1985).

In p r inc ip le , bo th the au togene t ic exc i ta t ione v o k e d th ro u g h th e g a mma lo o p a n d mo to n e u ro nd e p o la r i z a t i o n p ro d u c e d b y th e c e n t r a l c o mma n d

could exp la in per se the observe d fac i l i ta to ry e ffec t.However, the poss ib i l i ty tha t pe r iphera l a ffe ren tsac t iva ted dur ing movement migh t a l so con t r ibu tedeserves e ither a t ten t ion . In fac t , dur ing mos t o f thes tance phase , the So l musc le is subm it ted to cons ider-ab le s t re tch ing , which wil l fu r ther enha nce the exc i ta -to ry Ia inpu t ( see Got t l ieb and Agarwal 1979) .M o re o v e r, t h e ma x imu m a mp l i t u d e o f th e H - r e f l e x isa t ta ined concu rren t ly w i th the pu sh-off phase o f thes tep cyc le , whe n , d ue to iner t ia fo rce , a load h igherthan the body weigh t i s suppor ted on a s ing le l imb.Exper iments on f ree ly walk ing ca ts ind ica te tha tdur ing ana logous m echan ica l eve n ts , severa l c lassesof p ropr io - and ex te roce p tors w i th a po ten t ia lfacil i ta tory effect on the ankle extensors actuallydischarge (Loeb 1981), including: the load-sensit ivejo in t recep tors and group I I I musc le recep tors (Pear-son and D uysens 1976) ; the musc le sp ind les loca tedin the intr insic plantar muscles yielding a consistentexcita t ion of Sol a lpha M Ns in the digit igrade cat , butalso in the plantigrade primates (Hongo et a l . 1984);t h e l o w th r e s h o ld me c h a n o c e p to r s o f t h e fo o t s o l eand the cu taneou s recep tors o f the sk in over ly ing theca lcaneum a nd sens it ive to tang en t ia l s t re tch ing dur-ing foo t dors i f lex ion (Duysens and Pearson 1976;

Loe b 1981; Schieppati and C ren na 1984a).I t is conceivable that a s imilar bulk of potential ly

exc i ta to ry inpu ts migh t converge on the So l motornuc leus dur ing the s tance phase o f human locomo-t ion (and s tepp ing) , and conseq uen t ly con t r ibu te tothe re in forcement o f ank le ex tensor ac t iv i ty dur ingthe suppor t and the push-off phase o f the s tep cyc le .In ag reem ent w i th this hypothes is i s our f ind ing of ala rger p ropor t ion o f So l M N po pula t ion con t r ibu t ingto the s tance facil i ta t ion during the walking task ( inwhich the body weigh t i s ac tua l ly loaded on thetes ted l imb) as compared wi th the s tepp ing one ( inwhich no load ing wha tsoever occurs ) . In te res t ing ly, adetai led stud y by Pierrot-D eseil l igny et a l. (1983)per formed in man under s ta t ic condi t ions ind ica testha t in te rac t ion be tween cu taneous inpu t f rom thefoo t soles and Ia inpu t f rom gas t rocnemius and so leusmuscles is organized to provid e re flex actions assis t-ing bipedal gait , part icularly during the s tance phase .

En d s t ance - s w i ng i nh i b i t i on

An ac t ive inh ib i t ion o f var ious motoneurona l poo lsdur ing the s i len t phase o f the i r rhy thmic locomotor


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which are character ist ic of the second hal f of thes t ance phase . The hypo thes i s t ha t d i ff e ren t mecha -n i sms can modi fy t he r e f l ex t r ansmiss i on in d i ffe ren tphases of the step cycle , seems not contradic ted bythe above da t a .

Acknowledgements.The authors are very grateful to ProfessorsFausto Baldissera and Antonio Pedotti for commenting upon andreviewing the manuscript. Secretarial help by Miss Franca Marconis gratefully acknowledged. This work was supported by the PublicMinister of Education (M. P. I.) and Centro di Teoria dei Sistemi,Consiglio Nazionale delle Ricerche, Italy.

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3-15_Excitability of the Soleus H-Reflex Arc During Walking and Stepping in Man