median nerve section and resuture

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1 Journl of Neurology, Neurosurgery, nd Psychitry 1987;5: Ptterns of reinnervtion nd motor unit recruitment in humn hnd muscles fter complete ulnr nd medin nerve section nd resuture CHRISTINE K THOMS, RICHRD B STEIN, TESS GORDON,* ROBERT G LEE,t M GEORGE ELLEKERt From the Deprtments of Physiology, Phrmcology* nd Medicine,1 University of lbert, Edmonton, nd Deprtment ofclinicl Neurosciences,j University of Clgry, Clgry, Cnd SUMMRY Following complete ulnr or bove-elbow medin nerve sections, there ws no significnt correltion between motor unit size (twitch mplitude) nd recruitment threshold, s ssessed by spike triggered verging. This bsence of orderly recruitment ws ttributed to misdirection of motor xons during regenertion. Following medin nerve section t wrist level, where the reinnervted muscles hve more synergistic ctions, orderly recruitment by size ppered to be re-estblished. Thus, the size principle of motor unit recruitment cn be re-estblished fter nerve section in humns, if motor xons innervte their originl muscles or ones with closely synergistic functions. If we wnt to tie shoelce, write letter, et, or ply musicl instrument, we re confronted with the need to control our hnd muscles precisely. Our bility to co-ordinte these nd mny other fine movements is generlly ssumed to result from direct corticospinl connections to the motoneurons innervting the hnd muscles' 2 nd from n orderly recruitment of motoneurons from smll to lrge within ech spinl motor pool.34 One notble exception to this recruitment pttern occurred fter resuture of completely severed ulnr nerve in the forerm. Norml motor unit twitch mplitudes were re-estblished but the threshold force for recruitment of these reinnervted motor units remined bnorml. In ddition to disordered recruitment of motor units, these individuls showed poor motor co-ordintion for fine movements.5 In these ptients, the xons hd been severed nd so disconnected from pthwy to their peripherl end orgns. s the ulnr nerve contins xons which innervte severl intrinsic hnd muscles, mny muscles were denervted. During regenertion, the xons hd to grow cross the suture line nd long the endoneuril tubes to innervte the denervted muscle fibres ddress for reprint requests: Dr RB Stein, Deprtment of Physiology, University of lbert, Edmonton. lbert, Cnd. T6G 2H7. Received 22 pril ccepted 25 My in the periphery.6 These xons hd opportunities to reinnervte their originl or foreign muscles. Therefore, the disordered recruitment of reinnervted motor units could hve resulted from misdirection of motor xons to foreign muscles with different functions nd/or from chnges in the ctivity of the motoneurons. Studies on nimls hve shown tht severed motor xons do not reinnervte their originl muscles specificlly.7 Motor xons lso reinnervte muscle fibres irrespective of their originl type. This is reflected by the ltered distribution of the muscle fibres of reinnervted muscle units. They tend to be grouped together, rther tht scttered throughout the muscle in the norml mosic pttern.8 9 s most niml muscles re heterogeneous,1 these newly formed muscle units must contin fibres with different histochemicl composition nd contrctile properties. However, reinnervted motor units become like norml motor units with time, in tht their muscle fibres show homogeneous histochemicl composition"1 nd norml contrctile properties.'2 These chnges must hve involved trnsformtion of mny muscle fibres. Similrly, regenerting humn motor xons re unlikely to grow long their originl endoneuril tubes, lthough the pttern of motor innervtion in reinnervted humn muscles hs not been demonstrted. If reinnervtion is specific, chnge in the ctivity of the motoneurons could lter the threshold 259 J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

2 26 forces for voluntry recruitment of the motor units nd thereby produce disorderly recruitment within the reinnervted muscles. lterntively, non-specific reinnervtion of muscles could produce disorderly motor unit recruitment becuse of misdirection of motor xons from different motor pools. Even though size ordered reltionships between motor unit properties my be re-estblished in motor units which re ppropritely reinnervted by their originl motor xons, these reltionships my be obscured by the dt from misdirected motor units. Thus, the purpose of the present study ws to determine the pttern of innervtion nd recruitment of motor units in reinnervted humn hnd muscles fter complete severnce nd resuture of the ulnr nd medin nerve t different levels. Methods Clinicl ssessment Clinicl ssessments nd experiments were ll completed with the informed consent of the ptients nd ccording to the Declrtion of Helsinki. ll ptients (two femle, 11 mle; yers) hd ccidentlly severed the ulnr (six ptients) or medin (seven ptients) nerve in the pst 5 yers. Surgicl reports confirmed tht the nerves hd been completely sectioned nd surgiclly repired. ll nerve sections were t wrist level except for two bove-elbow medin nerve sections. The injured nerve nd tht of the control nerve in the other rm were ech electriclly stimulted t two levels to mesure xonl conduction velocity. bipolr needle electrode ws inserted percutneously into one or two reinnervted muscles in turn. The interference pttern ws exmined for the presence or bsence of norml nd polyphsic motor unit potentils. Muscle bulk nd strength, together with generl motor nd sensory function were ssessed cliniclly. Recruitment of reinnervted motor units Spike triggered verging13 ws used to record the twitch tension, contrction time, unrectified nd rectified EMG of the reinnervted motor units in reltion to the force t which they were recruited voluntrily. EMG ctivity Motor unit potentils were recorded with Dis bipolr needle electrode inserted percutneously into the first dorsl interosseous or bductor digiti minimi muscle of the ulnr nerve ptients nd into the bductor pollicis brevis or opponens pollicis muscle of medin nerve ptients (fig 1). Surfce EMG ctivity ws recorded with two Beckmn surfce electrodes positioned on the belly of the muscle. Force mesurements To mesure the force of voluntry muscle contrction from the first dorsl interosseous nd bductor digiti minimi muscles of ulnr nerve ptients, force trnsducer (Grss FT-3) ws positioned ginst the proximl interphlngel joint of the index nd little finger respectively. For the medin nerve ptients, two strin guges mounted t right ngles (for detils, see 14) were positioned ginst the nterior nd medil spects of the thumb interphlngel joint to record force from the bductor pollicis brevis nd opponens pollicis muscles respectively. Force from PB or OP FDI force Medin nerve Wrist nd finger flexors / Thoms, Stein, Gordon, Lee, Elleker Prontor teres } Needle EMG nerve EMG Fig I Schemtic digrm ol the pth of the ulnr nd medin nerves hel/ow the el/ow joint. s etch nerve trvels down the firerm nd into the hnd, it innervtes muscles with seprte motor pools nd diffrrent functions. The recording rrngement is onli illustrted for the hductor digiti minimi (DM) muscle. However, EMG from single motor units ws recorded with hipolr needle electrodes from the FDI or the DM muscle ier ulnr nerve section nd the hductor pollicis brevis PB or opponens pollicis (OP) muscle fier medin nerve section. Surfijce EMG ws recordedjfrom two electrode.s positioned on the belly of the respective muscles. Force ws recorded from the diferent muscles t the positions illustrted hy the solid hrs lthough only one or two trnsducers were used fir ech ptient. The first dorsl interosseous (FDI), DM, P nd other interossei nd lumbricl muscles were ll contrcted in turn to determine the originl motor pool of ulnrreinnervted motor units wheres the PB, OP, prontor teres (PT) nd wrist nd finger flexors were ctivted fir motor pool identifiction of medin-reinnervted motor unit.s. Spike triggered verging' Detils of the spike triggered verging technique hve been described erlier."3 Briefly, ech motor unit potentil ws ccurtely discriminted from the interference pttern (Bk Electronics Inc. window dis- J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

3 Ptterns ol reinnervtion nd motor unit recruitment in humn hnd muscles 261 crimintor) nd used to trigger progrmme on PDP I1/34 were plotted on logrithmic coordintes. Dt were lso computer to verge the force (filtered 11-1Hz), pooled nd plotted similrly for ulnr nerve nd medin unrectified nd rectified EMG (filtered 1-1, Hz) ssocited with the firing of the single motor unit. During ech 5 from subjects with normlly innervted hnd muscles. nerve sections. These dt were compred to those obtined sweep verge, the subject ws sked to recruit the motor Regression lines were fitted ccording to lest men unit nd fire it slowly but repetitively t force level ner to squres criterion.'9 Lines were computed which minimised the recruitment threshold (recorded continuously during the men squre devitions in the x-direction (x-line) nd the verging with digitl voltmeter) to minimise the distortion y-direction (y-line). The slope of the y-line is lwys the in the twitch profile.'5 l The verged unrectified nd smller of the two, nd ws used for sttisticl testing. This rectified EMG ws compred ' nd indicted the bsence of slope ws tken to be significntly different from zero t the synchronised motor unit ctivity during verging. 5% level when its vlue ws more thn fctor of two greter Ildentifiction ol the originl.spinl pool of motor units fter verging the reinnervted motor unit prmeters, the ptient ttempted to ctivte the sme motor unit by voluntrily contrcting different ulnr-innervted muscles in ulnr nerve sections (first dorsl interosseous, bductor digiti minimi, dductor pollicis, other interossei nd lumbricls) or different medin-innervted muscles in medin nerve sections (bductor pollicis brevis, opponens pollicis, wrist nd finger flexors, prontor teres; fig 1). Normlly innervted motor units were ctivted only by contrction of the muscle being recorded from. Reinnervted motor units tht showed the sme behviour were considered to be ppropritely innervted by motor xons from their originl motor pool. Those reinnervted motor units tht could be ctivted more esily by the contrction of other ulnr- or medin-innervted muscles fter the respective nerve sections, were considered to be reinnervted by motor xons from foreign motor pools. The originl motor pool for these motor units ws determined objectively from the muscle ction which resulted in the recruitment of the motor unit in the recording muscle t the lowest level of force nd rectified EMG. The ptients confirmed subjectively tht the motor unit ws ctivted with the lest effort by the contrction of tht muscle. Errors in this technique could rise when the respective muscles hve closely synergistic functions. For exmple, in the bductor pollicis brevis muscle, motor units cn be ctivted by bduction or opposition of the thumb. 8 Following medin nerve sections, these motor units were identified only s being of thenr muscle origin. Their ctions could be seprted clerly from those of the prontors nd wrist nd finger flexors. Similrly, the ulnr innervted first dorsl interosseous nd dductor pollicis muscles cn ct s synergists. However, s first dorsl interosseous motor units do not co-operte in dduction of the thumb without flexion of the index finger'4 motor units could be identified in these muscles by different muscle ctions. Procedure In turn, different motor unit potentils were discriminted by hving the subject exert vrious levels of voluntry force nd/or by repositioning the needle electrode in the muscle. The mechnicl properties of ech motor unit were verged nd the motor unit pool identified s outlined bove. One to three recording sessions of 1-2 hours were completed for ech ptient on different dys. nli.sis From the dt from ech ptient, grphs of the twitch tension mplitude, contrction time nd recruitment threshold thn the stndrd error of the slope. Regression lines were only drwn when they stisfied this sttisticl criterion. The line which hs slope equl to the geometric men (m-line) of the x-line nd the y-line ws lso computed nd ws drwn in the figures of this pper. This line is pproprite when comprble errors of mesurement occur in both the x- nd y-vlues nd is the line one would tend to fit by eye.'4 The numbers of motor units from the different identified spinl motor pools in the reinnervted muscles were pooled seprtely for ll ulnr nd bove-elbow medin nerve section ptients. clcultion ws mde of the contribution (%) of ech muscle to the newly formed spinl motor pools fter these different nerve sections. Results Clinicl ssessment The injured nerves typiclly hd lower conduction velocities thn those recorded from the control nerves in the contrlterl rm. The evoked compound muscle ction potentils were smller in mplitude nd more dispersed thn norml. In the reinnervted muscles, there ws generlly incresed EMG ctivity with needle insertion nd reduced interference pttern composed of both norml nd polyphsic motor unit potentils. Muscle strength nd bulk were sometimes less thn norml. Most ptients hd difficulty in isolting finger movements nd described chnges in their bility to complete fine motor skills such s fstening buttons nd picking up smll objects. Usully, tolernce to cold ws reduced nd tctile senstion ws impired. In ll ptients, the motor nd sensory deficits were specificlly confined to the typicl distribution of the nerve tht hd been injured. This suggested tht there were no vritions from the norml innervtion of individul muscles lthough this does occur occsionlly.6 Innervtion of reinnervted muscles The bductor digiti minimi, first dorsl interosseous nd bductor pollicis brevis muscles were reinnervted ppropritely by some of their originl motor xons nd inppropritely by motor xons tht hd previously innervted different muscles with different functions. Typicl exmples of the EMG ptterns of reinnervted motor units re illustrted in fig 2 for the bductor digiti minimi muscle. The second J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

4 262 Unit impulse rte ( Normlly directed motor unit I: DM surtfce EMG ctivte DM FDI P Misdirected motor unit Unit impulse rte DM surfce EMG 5s lo imp/s Fig 2 Unit impulse rte nd rectified surfce EMG ctivity of normlly directed () nd misdirected (b) motor unit recorded in reinnervted DM muscle. EMWG ctivity ws recordedfrom the DM muscle during contrction of either the DM, FDI or P muscles suggesting misdirection of mny motor xones to tht muscle. normlly directed unti () ws ctivted only by the contrction of the DM muscle. The motor xone hd therefore ppropritely reinnervted its originl muscle. The misdirected motor unit (b), ws ctivted most esily nd t the lowest level of DM rectified EMG by contrction of the FDI muscle so presumbly belonged to the originl FDI motor pool. trce, in fig 2, shows tht surfce EMG ctivity ws lwys recorded in the bductor digiti minimi muscle when the bductor digiti minimi, first dorsl interosseous or dductor pollicis muscles were ctivted. s norml subjects cn ctivte the bductor digiti minimi muscle independently of first dorsl inter- Tble Thoms, Stein, Gordon, Lee, Elleker osseous or dductor pollicis, this suggests tht mny motor xons hd been misdirected from other ulnr innervted muscles to the bductor digiti minimi muscle. Figure 2 lso shows n exmple of the typicl EMG pttern of normlly directed motor unit. The motor unit fired during contrction of the bductor digiti minimi muscle but ws silent during contrction of other ulnr reinnervted muscles such s the first dorsl interosseous or dductor pollicis. The motor xon hd therefore ppropritely reinnervted its originl muscle. In comprison, misdirected motor xons from foreign motor pools formed motor units which could be ctivted by voluntry contrction of other muscles innervted by the sme nerve (fig 2B). This motor unit ws recruited t the lowest level of bductor digiti minimi rectified EMG by contrction of the first dorsl interosseous muscle. Higher levels of bductor digiti minimi rectified EMG hd to be reched before the motor unit ws recruited by the ction of tht muscle or the dductor pollicis muscle. Therefore, the motor unit ws presumbly in the spinl motor pool of the first dorsl interosseous muscle prior to the nerve section, but grew bck to reinnervte muscle fibres in bductor digiti minimi. The tble shows the origin of the motor xons in the reinnervted muscles fter ulnr nd bove-elbow medin nerve section nd resuture. fter complete ulnr nerve section t wrist level, only 34% of the motor xons reinnervting the bductor digiti minimi muscle were from its originl motor pol. The remining motor xons hd been misdirected from the originl first dorsl interosseous (31%), dductor pollicis (18%) nd other interossei nd lumbricl (17%) motor pools. Similrly, 39% of the motor x-ons reinnervting the first dorsl interosseous muscle were from the originl first dorsl interosseous motor pool, wheres II, 22 nd 28% were from the bductor digiti minimi, dductor pollicis nd other interossei nd lumbricl motor pools respectively. fter medin Origin of motor xons in reinnervted muscles fter complete ulnr or medin nerve section nd resuture () Ulnr nerve sections t wrist level Motor units ctivted most esily by contrction of. First dorsl bductor digiti dductor Muscle interosseous minimi pollicis Others Totl bductor di*iti minimi First dorsl interosseous Totl 15 (31%) 22 (39%) 37 (36%) t6 (34%) 6 (11%) 22 (21%) (B) Medin nerve sections bove the elbow Motor units ctivted most esily by contrction of: 9 (18%) 12 (22%) 21 (2%) Muscle Thenr Prontor teres Flexors Others Totl bductor pollicis brevis 2 (48%) 2 (5%) 14 (33%) 6 (14%) 42 The numbers represent dt from six ulnr nd two bove-elbow medin nerve section ptients. 8 (17%) 16 (28%) 24 (23%) J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

5 Ptterns of reinnervtion nd motor unit recruitment in humn hnd muscles z E 1-4, V I E -c ui1 I.- 3r 1 3 1iL 21L 1 1 G) 14 _ Norml FDI muscle Reinnervted - 1 3r 1 o 2Q.,',' 1. -m */ FDI mussc le * o o o xons. Five, 33 nd 14% of the motor xons were from the prontor teres, wrist nd finger flexor or other motor pools respectively. Thus, these dt clerly show tht misdirection of motor xons occurs during reinnervtion. However, this my not be n entirely rndom process becuse in both the first dorsl interosseous nd bductor digiti minimi muscles, there ws some tendency to record from higher percentge of normlly directed motor units thn motor units from ny one foreign motor pool. Size reltionships in reinnervted muscles Figure 3 shows typicl exmple of the significnt positive correltion found between the size of the motor unit (twitch mplitude) nd the voluntry force t which the motor unit fired repetitively in normlly innervted first dorsl interosseous muscle (fig 3). Following ulnr nerve section t wrist level, the rnge of reinnervted motor unit twitch tensions nd recruitment thresholds ws comprble with norml vlues. However, the correltion between these two vribles ws not. significnt in n individul reinnervted muscle (fig 3B) or when dt were pooled o from severl reinnervted muscles (fig 3C). For normlly directed motor units (U) in the first dorsl inter- O osseous muscle, these correltions were positive but only significnt in one muscle studied. Dt recorded ( Reinnervted FDI mu! scles from reinnervted bductor digiti minimi muscles D showed similr trends. In normlly innervted bductor pollicis brevis muscle, significnt positive correltions were lso found between twitch tension mplitude nd recruitment threshold (fig 4). fter medin nerve section o * nd resuture t the elbow, these reltionships were not re-estblished in reinnervted muscle (fig 4C) or 1 *, when the dt from two muscles were pooled (fig 4E). o o... İo In normlly directed bductor pollicis brevis motor units (U) these reltionships were positive but not I I significnt. In comprison, when the medin nerve ws sectioned nd resutured t wrist level, the muscles Recruitment threshold were reinnervted by motor xons from motor pools ( N ) with closely synergistic ctions. Orderly reltionships Fig 3 Molor unit twvitch mplitude plotted g inst the between recruitment threshold nd twitch mplitude threshold.force of recruitment in normlly iniinervted FDI were re-estblished in reinnervted muscle (fig 4B) muscle (), one (b) nd,four (c) reinnervted FDI muscles or when dt from severl reinnervted muscles were fter ulnr nerve section nd resuture t wrist level. pooled (fig 4D). Different symbols represent normlly directed (U) nd mis- Figure 5 shows tht there were significnt negtive directed () motor units in ll grphs. Regresision lines correltions between motor unit contrction time nd minimising the devitions in the x nd y directiions re twitch mplitude in normlly innervted first dorsl drwn in these nd s'lbsequent figs only when thre interosseous nd bductor pollicis brevis muscles (fig reltionships were significntly different fromzero t the 5% level of confidence. S, 5B). Following ulnr or medin nerve section nd resuture, these correltions were wek (fig SC) or bsent (fig SD) in reinnervted muscles. The rnge of nerve section bove the elbow, 48% of the rein- contrction times recorded in reinnervted muscles nervted bductor pollicis brevis muscle motor pool ws similr to tht recorded in the respective norml ws formed by originl thenr (bductor pollicis muscles. However, in ll reinnervted muscles, the brevis, opponens pollicis, flexor pollicis b)revis) motor men motor unit contrction time ws fster thn 263 J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

6 264 z E 4' V ' E -c t 2 3I 1 1 S,III I z E 41 I.._ cl E._ _-.4 Wrist I,I I I I l Norml PB muscle Reinnervted Reinnervted,h PB muscle -,o PB muscles S 1 3 Thoms, Stein, Gordon, Lee, Elleker Elbow section 1 o O * I Recruitment threshold (N) Fig 4 Motor unit twitch mplitude versus recruitment threshold in normlly innervted PB muscle (). Dt re plottedfrom one (b, c) nd severl (d, e) reinnervted PB muscles fter medin nerve section t the wrists nd bove the elbow respectively. Normlly directed motor units (U) re represented by different symbol to reinnervted motor units with motor xones of undetermined origin () nd misdirected reinnervted motor units (). J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

7 Ptterns of reinnervtion nd motor unit recruitment in humn hnd muscles vs Ẹ. GD E c -) c Norml FDI muscle *u E II I 1I 2I Twitch mplitude (mnn) Fig 5 Motor unit contrction time plotted s function of twitch mplitude in normlly innervted FDI () nd PB (c) muscle. Dt re plotted for reinnervted FDI (b) nd PB (d) muscles fter ulnr nd bove elbow-medin nerve severnce nd repir respectively. norml, but the differences were not sttisticlly significnt. s the ptients sometimes found it difficult to ctivte single motor unit t low stedy frequency, the errtic dischrge pttern could hve resulted in n underestimtion of the contrction times for motor units. Discussion 1 6F * fter complete ulnr or medin nerve section nd resuture in humns, regenerting motor xons were shown here either to reinnervte their originl muscles or to be misdirected to foreign muscles. Only when motor xons reinnervte muscles with closely synergistic functions (medin nerve t wrist), re orderly size reltionships between motor unit properties re-estblished (fig 4B, 4D). Innervtion of reinnervted muscles The poor motor coordintion for fine movements observed cliniclly fter peripherl nerve section nd - 2 Norml U. Reinnervted PB muscle * *-^ & PB muscles repir nd the mss movements of fcil muscles fter fcil nerve injury hve sometimes been ssumed to result from misdirection of regenerting motor xons.2-23 In the present study, this ssumption ws substntited for peripherl nerve sections by identifying the originl spinl motor pool of reinnervted motor units following ulnr nd medin nerve section. In the reinnervted first dorsl interosseous, bductor digiti minimi nd bductor pollicis brevis muscles, two ptterns of motor unit ctivity were recorded. Some motor units could be ctivted only by the ction of the muscle in which they were recorded so they functioned normlly. Presumbly, the motor xons of these motor units reinnervted their originl muscle. Other motor units could be ctivted best by contrcting muscles innervted by the sme nerve. These motor units were presumbly formed by the motor xons being misdirected to reinnervte foreign muscle. It ws not tested to see if one xon innervted severl muscles, but this is unlikely since xon sprouting usully occurs over very short distnces J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

8 266 Similrly, the loction of the cell body in the spinl cord ws presumbly unltered. Following peripherl nerve section nd resuture in nimls, the loction of the cell bodies remin intct nd the motor xons exit from the pproprite ventrl roots.25 lterntive explntions could be offered for the bnorml motor unit ctivity observed here. These include: () ephptic trnsmission (b) ltertions in the synptic connections in higher brin centres (c) motor xons splitting to innervte different muscles. Impulses cn be generted ectopiclly in chroniclly injured nerve fibres nd possibly from hyperexcitbility of the membrne.2627 lthough this process my contribute to the motor unit ctivity recorded here, it seems unlikely tht the impednce mtching between the xons would be consistently pproprite to evoke trnsmission from locl currents. Monkeys28 nd cts hve been observed to perform well coordinted gol-directed movements fter crossunion of lrge common nerves in the forerm. fter deliberte cross-union of nerves, such re-eduction my result from compenstion by the ctions of synergistic muscles. In cts, the bility to perform coordinted voluntry movements my lso result from sprouting of corticorubrl neurons onto the proximl portion of the red nucleus.29 However in mn, the red nucleus nd the rubrospinl trct is less well developed.3 If synptic ltertions in these or other higher centres such s the corticospinl trct do occur in mn fter complete nerve section nd repir, they do not pper to permit well coordinted finger movements. The ptients in the present study reported difficulties in controlling their hnd muscles during some functionl tsks. Exmples of xon splitting hve been reported in the extroculr nd lumbricl muscles of the ct.3' 32 This phenomenon is rre in humn nerve regenertion. In some ptients who hve sectioned the ulnr (2/18, 11%) or fcil (1/5, 4%) nerve, synchronous ctivity of some motor units ws observed in different muscles reinnervted by the sme nerve.2 synchronous motor unit dischrges were much more common in ll muscles exmined, implying simple misdirection of the xon to foreign muscle, s is proposed here. From the present dt, reinnervtion of humn hnd muscles is clerly not specific. Similr findings hve been reported in rt muscles when motor xons were provided with choice of muscles to reinnervte.7 However, s more normlly directed motor units thn misdirected motor units from ny one foreign pool were recorded in the bductor digiti minimi nd first dorsl interosseous muscles fter ulnr nerve section, this would suggest tht reinnervtion is not n entirely rndom process either. The bductor digiti Thoms, Stein, Gordon, Lee, Elkeker minimi or first dorsl interosseous muscle cn be ctivted by different ctions to tht of the dductor pollicis muscle so units ctivted by these musc!e ctions re unlikely to be mistken with other motor pools. lterntively, the tendency for more normlly directed motor units to be recorded in these muscles my result from the creful remtching nd resuture of the severed fscicles during surgery. This my provide the regenerting xons with better opportunity to regrow long their originl endoneuril tubes. Similrly, if the nerve section is quite close to the point of entry of the individul nerves into the muscles, there will be fewer brnch points t which xons could be misdirected. The ctul rndomness of the reinnervtion observed here could be substntited by ntomicl informtion on the numbers of motor xons in the ulnr nerve t the wrist nd the respective muscle nerves, but this informtion is not currently vilble to our knowledge. Size reltionships in reinnervted muscles Following ulnr nd bove-elbow medin nerve section nd resuture, the regenerting xons cme from spinl pools with different functions. In the reinnervted first dorsl interosseous, bductor digiti minimi nd bductor pollicis brevis muscles, motor unit recruitment ws disordered. The ulnr nerve dt confirm the previous findings of Milner-Brown et l.5 Furthermore, the dt suggest tht the lck of orderly motor unit recruitment by size fter these complete nerve sections results from misdirection of motor xons from foreign motor pools. In contrst, fter medin nerve section nd resuture t the wrist, motor xons from synergistic motor pools reinnervted the denervted muscle fibres. Despite presumed misdirection of motor xons from foreign motor pools, orderly size reltionships between motor unit properties were found in the bductor pollicis brevis muscles. Thus, orderly motor unit recruitment cn be re-estblished fter complete nerve section nd resuture in humns, if the reinnervted muscles hve closely synergistic functions. One fctor fvouring recovery fter this injury my be the proximity of the section to the denervted muscle fibres. Ner the level t which muscle nerve leves the min nerve trunk to innervte muscle, the fibres of tht individul nerve re shrply loclised.6 With good fsciculr repir fter clen cut, misdirection of xons my be reduced. The reltionships found between recruitment threshold nd twitch mplitude in normlly directed motor units did show some tendency for norml reorgnistion nd orderly recruitment. However, even though the size reltionships for one muscle or one motor pool my be restored, these originl pools were dispersed between different muscles fter rein- J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

9 Ptterns of reinnervtion nd motor unit recruitment in humn hnd muscles nervtion becuse of misdirection of regenerting motor xons. Thus, recruitment in ny one muscle would depend on the recruitment of motor units from severl pools with different functions. This ws reflected by the difficulties the ptients hd in isolting individul finger movements. Typiclly, ll muscles innervted by the sme nerve would contrct to some extent. These inpproprite movements my result from orderly recruitment of motor units by size within the originl motor pools. Dt from niml studies support the proposl tht misdirection of motor xons rther thn chnge in icl the ctivity of the motoneurons my explin disordered recruitment of motor units nd poor muscle control fter complete nerve section nd repir in humns. Full recovery of motoneuron properties nd synptic contcts onto xotomised motoneurons occurs following muscle innervtion.33 When motoneurons reinnervte their former or ntgonistic muscles, the physiologicl reltionships between nerve nd muscle properties lso retumed to norml. Th-us, the tension nd contrctile speed of the muscle units were directly relted to the mplitude of the extrcellulrly recorded ction potentil, s found in normlly innervted muscles Self-reinnervted muscles function ppropritely during locomotion. In comprison, cross-reinnervted ct muscles typiclly fired ccording to the pttern expected of the innervting motor pool during locomotion.35-3 Therefore, these dt would tend to suggest tht even though nerve nd muscle unit properties re reestblished fter nerve section nd resuture, the motor units re recruited t level of force tht is pproprite within their originl motor pool s is proposed here. The impired sensory function of the ptients in the present study probbly results from berrnt sensory reinnervtion. Even though sensory xons reinnervte their end orgns specificlly, they re unlikely to reinnervte their originl mechnoceptor. Misguided fferent fibres hve been proposed to explin the perceptul misloctions of tctile stimuli following ulnr nd medin nerve section in humns38 39 nd the bnorml response chrcteristics of muscle fferents fter cross-reinnervtion of the ct soleus muscle.4 Thus, even though the fferent responds to n pproprite mechnoceptor, the loclistion of the sensory stimulus my be interpreted incorrectly. This mismtching of sensory connections my be distorted further by misdirection of the motor xons to foreign muscles. In conclusion, fter complete ulnr or medin nerve section nd resuture in humns, the reinnervtion of hnd muscles ws shown to be bnorml physiologiclly. Motor xons reinnervted their originl or foreign muscles. Even so, the reinnervted muscles 267 served some useful tunction during power or gripping movements. Finely coordinted movement sequences were impired, in prt due to misdirection of motor xons nd in prt to impired tctile senstion. Thus, the dt in this study not only emphsise the need for lrgely preserving the pttern of nerve nd muscle connections for size ordered motor unit recruitment, but lso show the importnce of this pttern of recruitment for control of fine movements. This reserch ws supported by grnts from the Med- Reserch Council of Cnd nd the Musculr Dystrophy ssocition of Cnd. CKT ws Commonwelth Scholr. References I Clough JFM, Kernell D, Phillips CG. The distribution of monosynptic excittion from the pyrmidl trct nd from primry spindle fferents to motoneurons of the bboon's hnd nd forerm. J Physiol (Lond) 1968;198: Lwrence DG, Kuypers HGJM. Pyrmidl nd nonpyrmidl pthwys in monkeys: ntomicl nd functionl correltion. Science 1965;148: Hennemn E, Somjen G, Crpenter DO. Functionl significnce ofcell size in spinl motoneurons. J Neurophysiol 1965;28: Milner-Brown HS, Stein RB, Yemm R. The orderly recruitment of humn motor units during voluntry isometric contrctions. J Physiol (Lond) 1973;23: Milner-Brown HS, Stein RB, Lee RG. Pttern of recruiting humn motor units in neuropthies nd motorneuron disese. J Neurol Neurosurg Psychitry 1974;37: Sunderlnd S. Nerve nd Nerve Injuries. London: Livingstone, Gillespie MJ, Gordon T, Murphy PR. Reinnervtion of the lterl gstrocnemius nd soleus muscles in the rt by their common nerve. J Physiol (Lond) 1986;372: Dubowitz V. Pthology of experimentlly re-innervted skeletl muscle. J Neurol Neurosurg Psychitry 1967;3: Krpti G, Engel WK. "Type-grouping" in skeletl muscles fter experimentl reinnervtion. Neurology 1968;18: rino M, rmstrong RB, Edgerton VR. Hindlimb muscle fibre popultions of five mmmls. J Histochem Cytochem 1973;21: Kugelberg E, Edstrom L, bbruzzese M. Mpping of motor units in experimentlly reinnervted rt muscle. Interprettion of histochemicl nd trophic fibre ptterns in neurogenic lesions. J Neurol Neurosurg Psychitry 197;33: Gordon T, Stein RB. Reorgniztion of motor-unit properties in reinnervted muscles of the ct. J Neurophysiol 1982;48: Stein RB, French S, Mnnrd D, Yemm R. New J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

10 268 methods for nlyzing motor function in mn nd nimls. Brin Res 1972;4: Thoms CK, Ross BH, Stein RB. Motor-unit recruitment in humn first dorsl interosseous muscle for sttic contrctions in three different directions. J Neurophysiol 1986;55: ndressen S, Br-On E. Estimtion of motor unit twitches. IEEE Trns Biomed Eng 1983;3: Clncie B, Bw P. Limittions of the spike triggered verging technique. Muscle Nerve 1986;9: Milner-Brown HS, Stein RB, Yemm R. The contrctile properties of humn motor units during voluntry isometric contrction. J Physiol (Lond) 1973;228: Ross BH, Thoms CK, Clncie B. Humn motor unit recruitment during sttic contrctions in different directions nd during dynmic unrestrined movement. Neurosci bs 1985;11: Sokolnikoff IS, Redheffer RM. In: Mthemtics of Physics nd Modern Engineering. New York: McGrw-Hill, Esslen E. Electromyogrphic findings on two types of misdirection of regenerting xons. Electroencepheogr Clin Neurophysiol 196;12: Ford FR, Woodhll B. Phenomen due to misdirection of regenerting fibres of crnil, spinl nd utonomic nerves. rch Surg 1938;36: Frueh BR. ssocited fcil contrctures fter seventh nerve plsy mimicking jw-winking. Ophthlmology 1983;9: Kimur J, Rodnitzky RL, Okwr S-H. Electrophysiologic nlysis of berrnt regenertion fter fcil nerve prlysis. Neurology 1975;25: Slck JR, Pockett S. Terminl sprouting of motoneurones is locl response to locl stimulus. Brin Res 198 1;217: Brushnk TM, Mesulm MM. ltertions in connections between muscle nd nterior horn motoneurons fter peripherl nerve repir. Science 198;28: Krnjevic K. Ephptic interctions: significnt mode of communictions in the brin. News in Physiologicl Sciences 1986;1: Rsminsky M. Ectopic impulse genertion in pthologicl nerve fibres. Trends in Neurosciences 1983;6: Brinkmn C, Porter R, Normn J. Plsticity of motor behvior in monkeys with crossed forelimb nerves. Science 1983;22: Thoms, Stein, Gordon, Lee, Elleker 29 Tsukhr N, Fujito Y, Od Y, Med J. Formtion of functionl synpses in the dult ct red nucleus from the cerebellum following cross-innervtion of forelimb flexor nd extensor nerves. Exp Brin Res 1982; 45: Crpenter MB. ntomy of the corpus stritum nd brin stem integrting systems. In: Hndbook of Physiololgy. The Nervous System. Bethesd MD: m Physiol Soc Sect 1. Vol : Crndell WF, Goldberg SJ, Wilson JS, McClung JR. Muscle units divided mong retrctor bulbi muscle slips nd between the lterl rectus nd retrctor bulbi muscles in ct. Exp Neurol 1981;71: Emonet-Dennd F, Lporte Y, Proske U. Contrction of muscle fibres in two djcent muscles innervted by brnches of the sme motor xon. J Neurophysiol 197 1;34: Sumner BEH, Sutherlnd Fl. Quntittive electron microscopy on the injured hypoglossl nucleus in the rt. J Neurocytol 1973;2: Gordon T, Stein RB, Thoms CK. Orgniztion of motor units following cross-reinnervtion of ntgonistic muscles in the ct hindlimb. J Physiol (Lond) 1986;374: Gordon T, Stein RB, Thoms CK. Innervtion nd function of hind-limb muscles in the ct fter cross-union of the tibil nd peronel nerves. J Physiol (Lond) 1986;374: Luff R, Webb SN. Electromyogrphic ctivity in the cross-reinnervted soleus muscle of unrestrined cts. J Physiol (Lond) 1985;365: O'Donovn MJ, Pinter MJ, Dum RP, Burke RE. Kinesiologicl studies of self- nd cross-reinnervted FDL nd soleus muscles in freely moving cts. J Neurophysiol 1985;54: Hllin RG, Wiesenfeld Z, Lindblom U. Neurophysiologicl studies on ptients with sutured medin nerves: fulty sensory locliztion fter nerve regenertion nd its physiologicl correltes. Exp Neurol 1981;73: Mckel R, Kunesch E, Wldhor F, Struppler. Reinnervtion of mechnoreceptors in the humn glbrous skin following peripherl nerve repir. Brin Res 1983;268: Gregory JE, Luff R, Proske U. Muscle receptors in the cross-reinnervted soleus muscle of the ct. J Physiol (Lond) 1982;331: J Neurol Neurosurg Psychitry: first published s /jnnp on 1 Mrch Downloded from on 6 June 218 by guest. Protected

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