In t r o d u c t i o n
P atient s w ith centr al nerv ou s sy st em (CNS ) disease u sually show gr eat difficulty bringin g their tibia ov er the support foot durin g the st ance phase of gait (P erry et al, 1974). Norm ally , a certain degr ee of t en sion in the triceps sur ae (dev eloped durin g st anding t o m aint ain upright st ance for postur al r egulation ) sh ould be ov er com e durin g w alking , su ch th at the body can pr ogr es s for w ar d (F un g and Barbeau , 1994). It is thought th at this limit ed ability , which patient s with CNS dy sfunction experien ce during w alkin g , is r elat ed t o an
impair ed m odulation of the spin al r eflex sy st em (Yang et al, 1991). Norm ally , the segm ent al r eflex es pr ovide the CNS with the m ean s t o r egulat e mu scle stiffness (Houk, 1979) and produce a proper adapt ation in the mu sculoskeletal sy stem (as a response to the changing envir onm ental con dition s).
T hese ar e know n t o be highly m odulat ed durin g mov em ent a s a fun ction of differ ent body position s (Capaday and St ein , 1986, 1987). Moreover , the amplitude of the H - r eflex is incr eased in patient s with CNS dy s - function (Sinkjaer et al, 1995; Yang et al, 1991) int erfering with their ability t o gate peripher al affer ent feedback during for w ar d
M u s c le E c c e ntric Co ntro l in Gait In it i at io n
K im H y e o n g - d o n g , M.H .S.
Dept . of Phy sicaI T her apy , Univ er sity of F lorida
국 문 요 약
보 행 시 작 시 원 심 성 근 육 수 축 조 절
김형동
플로리다 대학교 물리치료학과 박사과정
전시냅스 억제(presynaptic inhibition)와 동시냅스 억제(homosynaptic depression)는 보 행 시에 분절반사(segmental reflex )를 조절하는 두 가지 독립적인 기전이다. 근방추 피드 백(feedback)은 전시냅스 억제(inhibition )를 통해 보행 시 원심성 근육 수축기에서 적절이 조절될 수 있다. 이러한 전시냅스 억제 작용은 H - reflex의 강도로 나타내질 수 있는데, 원심성 근육 수축기 동안 H - reflex의 강도가 약해지는 것으로 보아 전시냅스 억제 작용 은 증가되는 것으로 보여진다. 근방추 구심성 피드백(feedback) 역시 동시냅스 억제를 통 해서 조절될 수 있다. 따라서 전시냅스와 동시냅스 억제는 보행 시작 중에 반사의 기전을 조절하는 중요한 역할을 한다. 반사의 조절 기전은 알파(alpha) 운동 신경원의 흥분도와 더불어 상위 척수의 기전들을 통해서 영향받고 조절된다. 경직성 마비 환자들은 초기의 입각기, 혹은 유각기 중에 손상된 비정상 비복근 H - reflex 조절기전을 보여준다. 이러한 비정상적인 조절기전은 발바닥의 말초신경을 자극함으로써 부분적으로 회복될 수 있다.
핵심단어 : 동시냅스 억제; 분절 반사; 원심성 근육 수축; 전시냅스 억제; H-r eflex .
pr ogr es sion (Yang et al, 1991). T his m ay be due t o int errupt ed descendin g input t o spinal int erneur on s as a r esult of an injury t o th e CNS (A shby an d McCr ea, 1987).
Durin g v olunt ary m ov ement the ov er all neural drive t o motor neur on s is contribut ed t o by both the supr aspin al contr ol an d spindle affer ent feedback (Matthew s, 1986), which in cr eases or decr eases the ov er all neural drive to the motor neuron s, accor din g t o the load on the mu scle (Burke et al, 1978; Matthew s , 1986). T hese changes in r eflex ex cit ability ar e a m echanism with which t o match the nervous command to the mechanical properties of the mu scle (Rom ano and Schieppati, 1987). During muscle isom etric and shortening muscle activation the efficacy of the ex cit at ory connection s bet w een th e Ia input s t o the m ot or neur on s is incr eased (the gain of the str et ch r eflex pathw ay ) in or der t o enh ance the ov er all neur al driv e.
T his mechanism appear s t o be appr opriat e in allowing the mu scle t o incr ease it s for ce by r ecruiting m or e m ot or unit s when the for ce w ould other wise decr ea se due t o th e decr ea se in mu scle length (Rom ano an d Schieppati, 1987). This result is in agr eem ent with the fact that during sh ort ening mu scle activation additional motor unit s are necessary t o ov er com e th e disadv ant ag e cau sed by the decr ease in the mu scle spin dle activity (owing t o a r elativ e unloadin g of th e slow er intr afu sal mu scle fiber s) (Burke et al, 1978; Rom an o and S chieppati, 1987).
During len gthening mu scle activ ation such as seen with the soleu s (which under goes an active lengthening activation during m ost of the st ance phase) the mu scle bein g activ at ed w ould pr oduce a gr eat er for ce
due t o th e incr ease in it s length an d t o the increase in it s lengthening velocity (Rom ano and Schieppati, 1987). T he synaptic effectiv - eness of the spin dle affer ent feedback t o the motor neurons becomes reduced pr ogr ess - iv ely in or der t o r egulat e the lev el of mu scle contr action (Rom an o and S chieppati, 1987).
Modulation of the pr esyn aptic inhibition is r eflect ed in the lev el of amplitude of th e H - r eflex at a con stant EMG lev el, so t ask - depen dent chan ges in the H - r eflex amplitude (such as w alking , st anding and running ) at a con stant EMG lev el ar e due t o the pr esynaptic inhibition . F or ex ample, durin g eccentric mu scle activ ation , th e pr e- synaptic inhibition should increase t o account for the low er amplitude lev el of H - r eflex at a con st ant lev el of EMG (St ein , 1995).
Homosynaptic depression is another m ech a - nism responsible for gating primary affer ent s feedback (Curtis an d Eccles , 1960). In pathological condition s th e decr ease in h om osynaptic depr ession s is r espon sible for the decr eased vibr at ory inhibition in spastic patient s (Nielsen et al, 1993). It m ay r esult in the ex agger ation of str et ch r eflex es (m ay be inv olv ed in the pathophy siology of spasticity ) (Nielsen et al, 1993).
T hese t w o neur al mechanism s ar e func- tionally import ant durin g w alking , especially during gait initiation. The disruption in such mechanisms, which is shown in the patient s such as spinal cor d injury (SCI) and multiple sclerosis (MS ), int erfer es with their for w ar d pr ogr es sion during w alkin g (Yang et al, 1991). Norm ally , in the early part of the st ance phase, a s the ankle dor siflex es an d the body progresses forward (soleu s mu scle
lengthens), the soleus H- r eflex is depr es sed in n orm al in dividuals. T his m ay pr ev ent excessive reflex activation from the incr eased spindle affer ent feedback a ssociated with the eccentric len gthening of triceps sur ae as it is str etched (Yang et al, 1991).
How ev er , in m any patient s, the incr eased reflexes at this period produce large str etch - induced r espon ses which int erfer e with the sm ooth for w ar d adv ance ov er the body and tibia (Yang et al, 1991). During the swing phase in n orm al subject s the low H - r eflex amplitude, w hich r epr esent s the in cr eased pr esynaptic an d r ecipr ocal inhibition , allow s the ankle to dorsiflex without any int erfer ence fr om the str et ch - induced str ong r eflex of the triceps surae. In contrast , patient s whose r eflex m odulation is impair ed such as S CI or MS show abnorm ally activ e r eflex es, r esulting in difficulty clearing the foot ov er the gr ound (Sinkj aer et al, 1995; Yang et al, 1991).
T he purpose of this paper is t o det ermine and r eview the fact or s that contribut e t o the n eur al contr ol of the eccentric mu scle activ ation durin g gait initiation . F ir st , th e m odulation of segm ent al r eflex es will be studied, followed by the presynaptic inhibition and finally homosynaptic depression . S econd, clinical implication s w ill be discu ssed.
T he s eg mental reflex during m ov em ent Segmental stretch r eflexes serve t o supply the CNS with both a contr ol of mu scle stiffn ess, and a r apid adaptiv e r ole t o chan ging envir onm ent al con dition s (Houk , 1979). Chang es in the gain of str et ch r eflex can occur independent of the level of mu scle activ ation an d loadin g (Akazaw a et al,
1982; Capaday and St ein , 1986; Koceja et al, 1995). T his m echanism allow s the body to transfer smoothly during gait. The m odulation of the str etch r eflex g ain can be v aried when subject s chang e their position s (Katz et al, 1988; Miyake et al, 1984). At equal stimulu s int en sities and backgr ound EMG activ ation , the amplitude of the H - r eflex is lar ger during standin g as compar ed t o w alking (Capaday and St ein , 1986; Cr enna and F rigo, 1987). In addition , the amplitude of H - r eflex is low er durin g a standin g position as compar ed t o a sittin g position (Kat z et al, 1988). Koceja et al (1993) r eport ed that the amplitude of the soleu s H - r eflex is decr eased 16% durin g a quiet st anding as compar ed t o the pr on e position . Capaday and St ein (1987) pr oposed th at the soleus segmental stretch r eflex is depr essed as a fun ction of an incr ea sed postur al in st ability . F or ex ample, in hum an s during beam w alking , low er r eflex gain w as achiev ed, as compar ed t o n orm al tr eadmill w alking (Liew ellyn et al, 1990). A s t ask complexity incr ea ses, fu sim otor driv e is also in cr eased (Kocej a et al, 1995), but at the sam e tim e the segment al r eflex gain appear s likely t o be r educed in or der t o m aint ain an appr opriat e lev el of mu scle activation and stiffness. Through this m echanism , both the appr opriate lev el of mu scle activation and mu scle stiffness ar e achiev ed.
F or ex ample, durin g st anding , which is view ed as a st atic postur e, the depr ession of the soleu s str et ch r eflex (r educed r eflex gain ) is pr oduced t o pr ev ent a satur ation of the primary afferent feedback from occurring or fr om developing inst ability (Koceja et al, 1995; St ein and Capaday , 1988).
T her efor e, th e r educed m odulation of the soleus H- reflex becomes greater in pr oportion t o the gr eater degr ee of postur al in st ability . T his occur s becau se the in cr ease in the v elocity of postur al sw ay , du e to the r educed base of support , pr ovides a gr eat er mu scle spindle dischar g e. A s a r esult , the decr ea sed gain of th e segm ent al r eflex is needed (Koceja et al, 1995). In pathological conditions, the importance of this mechanism t o stability in st an din g is evident when the inability to m odulate the segm ent al str et ch r eflex in a con dition oft en seen in the patient population may cr eate a dest abilizin g oscillation, as well as a difficulty r esponding and adapting t o postur al perturbation s in st anding (Kocej a et al, 1995; Maurit z et al, 1979).
An incr eased pr esyn aptic modulation of the Ia affer ent s t o th e alpha m ot or neur on is closely r elated t o the decr eased lev el of soleu s H - r eflex (Yan g et al, 1991). During the w alking cy cle, the amplitude of the soleu s H - r eflex is str ongly m odulat ed (Capaday and Stein , 1986). Capaday and St ein (1986) found that th e H - r eflex w a s increased rapidly t o a maximum level durin g st ance in or der to a ssist in maint ainin g the upright position of the body against gr avity and ev entually lifting th e body off the gr oun d. In addition , aft er the t oe- off ph ase of the stance limb it was abruptly decr eased t o a low v alue (Capaday an d St ein , 1986).
During the swing phase the r eflex es w er e sm allest or ab sent w hile att empting t o oppose ankle dor siflexion (Capaday an d St ein , 1986).
P re s y n apt ic inhibition
T he changes in pr esynaptic inhibition of the la affer ent on the m ot or neur on s ar e r espon sible for gating spin dle affer ent feedback . T he pr esyn atic inhibition of the la affer ent s to mot or neur on s of the contr acting mu scles is decr eased (Hulborn et al, 1987). Hulborn et al. (1987) dem on str at ed that such a decr ea se in the pr esynatic inhibition to the contr acting mu scle allow s the la activity to contribut e t o th e ex cit ation of v olunt arily activ at ed motor neurons (the increase in the effectiv enes s of the mu scle spin dle feedback ). In contr a st , th e pr esyn aptic inhibition of the la afferent s to mot or neuron s of the uninv olv ed mu scles is incr eased (Hulborn et al, 1987).
T he incr ease in th e pr esynaptic inhibition on the Ia affer ent s t o m ot or neur on s of the uninvolved muscles might prevent the m ot or neur on s of th ose mu scles fr om being activ at ed, permitting th e pr oper r ole of the ant agonistic mu scle activ ation (Hulborn et al, 1987).
At the beginnin g of the v olunt ary m ov e- m ent contr action the pr esyn aptic inhibition of the Ia affer ent s to the m ot or neur on s is decr ea sed, r esulting in the in cr ease of the gain of the monosyn aptic str etch r eflex (Meunier an d Pierr ot - Deseilligny , 1989). A descendin g inhibition of presynaptic int er - neurons, which is alr eady established at the on set of m ov em ent , might contribute to a decrease in pr esynaptic inhibition (Meunier and Pierrot - Deseilligny, 1989). The descending contr ol selectively inhibit s those int erneur on s which ar e the mediating presynatic inhibition of the la affer ent s (which pr oject t o voluntarily activated motor neurons) (Meunier
and Pierr ot - Deseilligny , 1989). Lat er , as the pr esynaptic inhibition is incr eased, th e g ain of the r eflex is decr eased (Meunier and Pierr ot - Deseilligny , 1989).
Chang es in pr esyn aptic inhibition ar e centrally pr ogr ammed (Meunier and Pierr ot - Deseilligny , 1989). Hulborn et al (1987) described the changes in the pr esynaptic inhibition of the Ia affer ent s t o m ot or neur on s as bein g supr aspin al contr ol in origin and serving as an aid in achieving a selectivity of the mu scle activ ation in or der t o in cr ease the m ot or contr ol. A dditionally , at the beginning of a m ov em ent , a high gain m ay be an adv ant ag e which allow s the monosynaptic reflex to compensate r apidly for the actual load (becau se th e actual load is n ot y et decided at the initial ph ase of movement ) (Meunier and Pierr ot - Deseilligny , 1989). Later , the decr ease in the gain m ay be necessary in or der to prevent oscillation s fr om building up (Meunier and Pierr ot - Deseilligny , 1989).
In pathological condition s such as seen in S CI patient s, and MS patient s with spasticity , the r educed presynaptic inhibition of the la prim ary affer ent fiber s is r espon sible for hyper activ e t endon and H - r eflex es (Nielsen et al, 1993; Sinkjaer et al, 1995; Yan g et al, 1991). T h er efor e, with the impaired or reduced presynaptic inhibition dir ect ed at the Ia affer ent termin als these patient s m ay hav e a higher r eflex gain contributin g t o the clonu s en count er ed durin g w alking (Yang et al, 1991). At similar backgr oun d lev els of soleu s activity these patient s show a gr eat er soleu s H - r eflex amplitu de in w alkin g th an during st anding (Fung and Barbeau , 1994). T hese
patient s ev en show a gr eat er amplitude of the soleu s H - r eflex durin g midswin g th an in the static unloading position at the sam e degr ee of joint angle (F un g and Barbeau , 1994). T he m anifest ation of spasticity th at ev entually leads t o the ex agger at ed str et ch r eflex es and clonu s shown in the CNS patient s is r eflected in th e r educed spinal pr esynaptic inhibition (Burke an d A shby , 1972; Delw aide, 1973; Fung an d Barbeau , 1994; Pierr ot - Deseilligny and Mazier es, 1985).
H o m o s y n aptic depre s s io n
T he depr es sion of the soleu s H - r eflex t ends t o last for sev er al seconds when it is elicit ed by any of the follow ing : a slow passiv e str et ch of the soleu s mu scle, short - lasting vibration of the Achilles t endon , and/ or a pr eviou s v oluntary contr action (Cr one and Nielsen , 1989; Kat z et al, 1977).
T his post - activ ation depr ession , which is ev oked ex clu siv ely by either the str et ched or the activ at ed mu scle (not in other mu scles), appear s t o be cau sed by homo- synatic depr ession w hich is the lon g - lasting depression of the spinal m on osynaptic tr an smission (Curtisa and Eccles, 1960;
Balleg aar d et al, 1991). T his depr ession is due to a decr ease in synaptic tr an smission in the sen sory n eur on s aft er the activ ation of r eflex pathw ay s (Capek an d E splin , 1977).
Nielsen et al (1993) r eported that post - activation depression of the soleu s H - r eflex , which is ev oked by a slow passiv e str et ch of the soleu s mu scle, is significantly sm aller in S CI patient s than in h ealthy subject s.
This suggest s reduced hom osyn aptic depr es - sion . A decr eased post - activ ation , likely
cau sed by a m echanism similar t o th e hom osyn aptic depr ession , will r esult in an ex agg er ation of the str et ch r eflex (Nielsen et al, 1993). In other w or ds, the r educed hom osyn aptic depr ession may in cr ease the r eflex gain . In addition , the incr eased r eflex gain w ould dev elop a gr eat er mu scle acti- vation (increased level of muscle activ ation ).
A good ex ample is the fact that the hom osyn aptic depr ession is responsible for controlling the effectiv enes s of the mu scle spindle la affer ent feedback .
Clinic al im plic ati on
Spastic par etic patient s show the impair ed soleu s H - r eflex m odulation in the initial st ance phase or during the swing phase as a r esult of spin al cor d or head injury as compar ed to n orm al subject s (Yan g et al, 1991). In n orm al subject s th e H - r eflex should be low during the early st an ce and swing phase. A low H - r eflex allow s the tibialis anterior activity and ankle dor siflex on m ov em ent t o be un opposed by the str et ch r eflex ev oked in the triceps sur ae (Capaday and St ein , 1986). In contr ast , spastic S CI patient s show abnormal activity in the silent phase of the gait cy cle such a s triceps sur ae bur sting , and ev en triggering clonu s (F ung an d Barbeau , 1994). T his is owing to a defective Ia regulatory m ech anism r esulting fr om th e disruption of supr aspin al and/ or pr opriospinal influen ce (Yang et al, 1991). Yang et al.(1991) r eport ed that an inadequate control of the presynaptic inhibition that t erminat es at Ia affer ent t erminals m ay be r espon sible for a diminished or ab sences of H - r eflex modulation ob serv ed in spastic paretic subject s. In those cir cum -
st ances th e spindle affer ent s feedback of the triceps sur ae incr eases con sider ably leadin g t o th e ex ag ger at ed str etch r eflex es and clonus and making the forwar d adv an ce of w alking difficult (F un g et al, 1990; Yang et al, 1991).
T he abnormal Ia m odulat ory mechanism s which occur during w alking can partially and artificially be restored by the application of a peripher al stimulu s t o the sole of the foot , pr ovided th at the segment al cir cuitry r em ain s intact (F un g and Barbeau , 1994).
The underlying segmental mechanisms, w hich ar e r espon sible for th e conditionin g inhibi- tion of an otherwise ex cessive H - r eflex in the early st ance an d swing ph ases of gait (in spastic SCI patient s), are pr esynaptic an d post synaptic inhibition . In par aplegic patient s a significant and r egular decr ease of the het er onym ou s Ia facilit ation w as ob serv ed fr om the quadriceps and soleu s when the flex or r eflex affer ent stimulation ev okes pr esynaptic inhibition t o Ia tr an smis sion (and then t o alpha m ot or neur on s) (Roby - Br ami an d Bu s sel, 1990). T his r esult str ongly suggest s that the pr esynaptic inhibition can be m ediat ed by intr aspinal m echanism s . In addition , the fun ctional or ganization of the spinal cor d in S CI patient s is similar t o that seen in an acut e spinal cat inject ed with DOPA (Jank sw ska et al, 1967). It is highly possible th at the intraspinal mechanism by which pr esynaptic inhibition is mediated is similar to a depolari- zation of both the ipsilateral (Ander son et al, 1986) and contr alat er al (Jank sw ska et al., 1967) Ia t erminals of the acut e spin al cat injected DOPA .
In or der to adv ance the body for w ar d
durin g w alking , an ex ces siv e soleu s str et ch mu st be r em ov ed in or der to m aint ain a compliant int erface bet w een the body and the gr ound (Capaday and St ein , 1986; St ein and Capaday , 1988). Con sequ ently , one of the goals of the r ehabilit ation for CNS patient s is t o inhibit the abnorm al r eflex segm ent ally in th e spastic par etic subject s durin g g ait (F ung and Barbeau , 1994).
Under these circumstances cutaneous stimula - tion can be applied t o r est ore some adaptiv e contr ol of gait in subj ect s with spastic mu scle activ ation (F ung and Barbeau , 1994;
Yan g et al, 1991).
S u m m a r y
T her e ar e tw o independent m echanism s t o contr ol the segment al r eflex gain in hum an s during g ait . T hey ar e pr esynaptic inhibition an d h om osynaptic depr ession . T hr ough the mechanism of the pr esyn aptic inhibition, the muscle spindle afferent feedback can be pr operly gat ed during eccentric phase of gait . T he m odulation of th e pr esynaptic inhibition is r eflect ed in th e lev el of H - r eflex at a con st ant EMG lev el.
During the eccentric mu scle activ ation pr esynaptic inhibition should incr ease t o account for the low er amplitude lev el of H - r eflex at a con st ant lev el of EMG.
Homosynaptic depression is another m echa - nism respon sible for regulating the effectiv - eness of the muscle spindle afferent feedback . Both the pr esynaptic inhibition and th e m onosyn aptic depr ession ar e r espon sible for modulating reflex gain during gait initiation . Reflex m odulation is influenced not only as a passiv e con sequen ce of the alpha mot or
neur on ex cit ation lev el, but also thr ough supr aspinal m echanism s. Spastic par etic patient s sh ow the impair ed soleu s H - r eflex m odulation either during the initial st ance phase, or during the swin g phase. T his abnormal modulatory mechanism can partially and artificially be restored by the application of peripher al stimulu s to the sole of the foot , pr ovided th at the segment al cir cuitry r em ain s functional.
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