Electrophysiological of motor monkey extensor digitorumUniversitg de Montreal, Montreal, Que'bec, Canada SUMMARY The electrophysiological technique used to estimate the number of motor

Journal ofNeurology, Neurosurgery, and Psychiatry, 1977, 40, 756-764

Electrophysiological and anatomical estimation ofthe number of motor units in the monkey extensordigitorum brevis muscleJEAN-MARIE PEYRONNARD AND YVES LAMARRE

From the Centre de Recherche en Sciences Neurologiques, De'partement de Physiologie,Universitg de Montreal, Montreal, Que'bec, Canada

SUMMARY The electrophysiological technique used to estimate the number of motor unitsin man (McComas et al., 1971b) was tested in six monkeys. The number of motor units wasestimated electrophysiologically in the extensor digitorum brevis (EDB) after deafferentation byexcision of the lumbo-sacral dorsal root ganglia. In five animals, the mean number of motor unitsobtained by the technique was in good agreement with the number of alpha motor fibres countedin the nerve to EDB. However, the results obtained in one animal with partial denervation of theEDB indicate that the technique might be unreliable, at least at certain stages, after aperipheral nerve lesion.

McComas et al. (1971b) described an electro-physiological technique to estimate the numberof motor units in the extensor digitorum brevismuscle (EDB) of man. They observed that smallgraded changes of the electrical stimulus to thedeep peroneal nerve at the ankle induced an in-cremental response in the evoked action potentialof the EDB. Assuming that each increment ofvoltage was due to the excitation of one motorunit, they divided the average amplitude of theincrements into the M response evoked by amaximal nerve stimulation to obtain the approxi-mate number of motor units within the muscle.Findings by this technique indicated a loss offunctioning motor units in patients suffering fromvarious types of muscular dystrophies (McComaset al., 1971a; McComas et al., 1971c; Sica andMcComas, 1971), myasthenia gravis (McComaset al., 1973a), as well as in hemiplegic (McComaset al., 1973b) and elderly subjects (Campbell et al.,1973).However the validity of the technique has been

questioned (Feasby and Brown, 1974; Brown andMilner-Brown, 1976), and doubts have been ex-pressed regarding the significance of the resultsobtained in patients (Engel and Warmolts, 1973;Panayiotopoulos et al., 1974).This work was supported by grants from the Medical Research Councilof Canada. YL is a member of the MRC Group in NeurologicalSciences at the Universit6 de Montreal.Accepted 7 February 1977

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In order to test the accuracy of the motorunit counting technique, attempts have been madein man (McComas et al., 1971b) and animal (Eisenet al., 1974) to compare electrophysiologicalevaluations of the number of motor units in amuscle to histological counts of alpha fibres inthe motor nerve. However, such an approach islimited by the difficulty of estimating the pro-portion of sensory and motor fibres in non-deafferented nerves. For this reason, we have usedthe technique of McComas in the present study todetermine the number of motor units in both thenormal and deafferented EDBs of monkeys, andwe have compared these estimates with the histo-logical counts of alpha motor fibres in the deepperoneal nerve, which supplies this muscle.

Methods

The experimental animals were Macaca mulatta.In these monkeys as in man the EDB is suppliedby the deep peroneal nerve which divides at theankle into two branches: the purely sensorymedial branch which innervates the skin of thefirst interdigital cleft, and the lateral motorbranch, which supplies the EDB and occasionallysends a terminal twig to the dorsal interosseousmuscles (Fig. 1). Preliminary experiments showedthat only L6 and L7 motor roots conitributed tothe innervation of the EDB (Fig. 2).

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Electrophysiological and anatomical estimation of motor units

/. DEEP PERONEAL NERVE

MOTOR BRANCH....... SENSORY bRANCHTO E.D.B.

E.D.B....

TERNAL BRANCH.TO FIRST D.I.-

Fig. I Diagram m atic represenitaticoni of term iinaldistribution of deep peronieal nerve in the nlotkev.EDB. extensor digitorumni brevis: DI. dorsalinlteros seoiis.

.I-

LL

7

10 ms

Fig. 2 Potentials evoked in EDB after supramaximiialventral root stimulationi. Only, L6 and L7 cotntributedto motor innervation of the m ustcle. Negativity isupward.

SURGICAL 'ITECHNIQUESix adult animals (PA, PB, PD, PE, PF, andPG) of both sexes were anaesthetised with anintravenous injection of sodium pentobarbitone.Under sterile conditions a lumbo-sacral laminec-

tomy was performed on the right side. The duramater was opened and the L5, L6, L7, and SIdorsal roots were sectioned. Each dorsal rootganglion was isolated from the ventral root fibresand removed. Before returning the animals to theircages, the deafferented leg was protected by aboot made of gauze and rubber bands extendingup to mid-calf.

ELECTROPHYSIOLOGICAL TECHNIQUE

Before each recording session, the animals wereanaesthetised with sodium pentobarbitone injectedintraperitoneally. The protective boot was takenoff and the sk.in shaved and cleaned. The stimulat-ing electrodes consisted of a pair of silver screwspadded with felt soaked in a sodium chloridesolution (0.9 C ). They were inserted in a plasticholder 12 mm apart and positioned on the skin atthe ankle over the deep peroneal nerve, thecathode being distal to the anode. A stimulator(DISA Multistim) was used to deliver rectangularpulses of variable voltage and 50,s in duration ata frequency of 0.5 Hz.The surface recording electrodes were made of

thin silver strips 25 mm long and 5 mm broad,coated with conductive jelly. The active electrodewas placed on the endplate zone of the musclewhere the amplitude of the evoked response wasmaximal and its latency shortest. The referenceelectrode was attached to the sole of the footand an earth (ground) electrode was placedaround the leg.The muscle responses were amplified, recorded

on a storage oscilloscope, and photographed. Thecontours of the potentials were carefully drawnon transparent graph paper. In monkeys, as inman, a gradual increase in the strength of stimula-tion to the deep peroneal nerve at the ankleevokes a gradual increase in the response recordedin the EDB. Near threshold the increases inresponse are 'all or nothing' increments presumedto arise from the recruitment of individual alphamotor axons. However, above the level of the'maximum incremental response' these steps arenot distinguishable. Figure 3 is an example ofrecordings made during one session. In order tocalculate the mean motor unit voltage, the peakto peak amplitude of the largest incrementalresponse (in this case 954 iLV) was divided bythe number of increments (10). The number ofmotor units (88) was obtained by dividing themean motor unit amplitude (95.4 ,uV) into theamplitude of the muscle response evoked bysupramaximal stimulation (8.4 mV). In fiveanimals (PA, PB, PD, PE, PF) these measure-ments were repeated three to 23 times during each

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Jean-Marie Peyronnard and Yves Lamarre

,r erne in cJ ., es ) c r es

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Fig. 3 Incremental responses of EDB afterstimulation of deep peroneal nerve at or slightly abovethreshold intensity (upper record) and supramaximalintensity (lower record).

of the four to five recording sessions (Table 1).The first recordings took place three weeks afierdeafferentation which allowed enough time fordegeneration in case of accidental injury to somemotor root fibres during surgery. The last record-ings were obtained on the day of sacrifice, that isfive to 11 weeks after the operation. In oneanimal (PG) who sustained a severe L7 ventralroot lesion during the process of deafferentation,nine recording sessions were carried out over apostoperative period of 12 weeks.

HISTOLOGICAL TECHNIQUEThe anaesthetised animals were perfused with a3% solution of glutaraldehyde in buffered 0.1 Mphosphate. The deep peroneal nerves were dis-sected from mid-calf to their termination. In twoanimals (PB and PF) a terminal branch ending in,the dorsal interosseous muscles, was found but itwas not looked for in one animal (PA). To verifythe completeness of deafferentation, two sensorynerves were removed, the sural and the terminal

branch of the superficial peroneal nerve. Theroots and spinal nerves were also dissected to beexamined for residual dorsal root ganglion cells.The nerves were cut in pieces approximately1 mm in length, post-fixed in 2% osmic acid, andprepared according to standard techniques forinclusion in Epon. Thin sections were stained withparaphenylenediamine, examined by phase micro-scopy and photographed. The fibre size histogramof the motor branch of the deep peroneal nervewas obtained from enlarged photomicrographs(X 1000) using a particle size analyser (ZeissTGZ3). Seven different levels were studied on theright deafferented side, from the ankle to themuscle in order to evaluate the incidence ofaxonal branching. On the left normal side, fibresize histograms were constructed at three differentlevels.

Reslts

RIGHT DEAFFERENTED EDB

Electrophysiological estimates of the number ofmotor unitsThe results from all recording sessions werepooled for each animal and the average numberof motor units (+ one standard deviation) wasfound to be respectively: 97+20 (PA), 92+17(PB), 86+17 (PD), 99-+115 (PE), 65+i=13 (PF).The values obtained on different recording

sessions for each of the five animals are presentedin Table 1. The variations which are seen onsuccessive sessions show no obvious systematictrend. The discrepancy between the largest andthe smallest estimates ranged from 19% (PE) to43% (PF) with an average of 32%. In the animalwith severe L7 ventral root lesion (PG) there wasa marked difference between the first and the lastsession. The estimated number of motor units wasinitially low (35+2) and increased progressivelyto a final value of 102=+-19 twelve weeks after theoperation (Fig. 4).

Table 1 Mean number of motor units in EDB right side-after deafferentation

Recording sessions

Animal ANo. I No. 2 No. 3 No. 4 No. S Average

PA 72±16 117+7 85+6 99±8 92±25 97±20n: 5 n: 10 n: 10 n: 11 n: 3 n:39

PB 90+8 95±19 81±7 124±8 92±17n:7 n:7 n: 12 n:4 n: 30

PD 79±13 85±12 81±9 91±11 104±8 86±17n:23 n: 10 n: 17 n: 17 n: 15 n:82

PE 92±13 100+16 114±8 94±11 99±15n: 17 n: 17 n: 11 n: 16 n:61

PF 86±5 68±11 49±3 54±5 63±6 65± 13n: 11 n: 15 n: 16 n:9 n: 14 n:65

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Electrophysiological and anatomical estimation of motor units 759

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small myelinated fibres (2-3 ,um in diameter) wereobserved. It is unlikely that they represent regen-erating fibres, because such fibres could not havereached the ankle even after a period of 12 weeksif one accepts the growth rate of axons to be2.5 to 3.5 mm/day (Gutmann et al., 1942), sincethe distance between the operated spinal rootscontributing to the nerve and the ankle is about350 mm. Furthermore, they were observed in oneanimal killed only five weeks after the operation.They may, therefore, represent postganglionicsympathetic myelinated fibres or else residualafferent fibres with cell bodies located very distallyin the proximal part of peripheral nerves (Cogge-shall et al., 1974) since no ganglionic cells werefound in serial sections of roots and spinal nerveson the operated sites. The ventral root fibresseemed well preserved with the exception of theanimal PG in whom one root (L7) supplying theEDB had been severely injured during the surgicaldeafferentation and showed no signs of regenera-tion (Fig. 6).

0 10 20 30 40 50 60 70 80

DAYS AFTER DEAFFERENTATION

Fig. 4 Estimated numbers of motor units in EDBmuscle of monkey PG at different times afterdeafferentation.

Histological counts of the number of alpha motorfibresHistological examination confirmed that, afterdeafferentation, there were no residual large affer-ent myelinated fibres left in the sensory nervesexamined. In some of them, such as the sensorybranch of the deep peroneal nerve (Fig. 5), a few

DEEP PERONEAL NERVEMOTOR

ANIMAL PGL 7 VENTRAL ROOT

DEEP PERONEAL NERVE

SENSORY

10 WEEKS AFTER DEAFFERENTATIONFig. 5 Light micrographs of sections from deepperoneal nerve in one of the deafferented animals(PE). There are no large myelinated fibres remainingin the sensory branch in contrast to the motor branch.

12 WEEKS AFTER DEAFFERENTATION

Fig. 6 Light micrographs of sections from injuredventral root L7 and from motor branch to EDB inanimal PG.

114ANIMAL PG

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In all cases, the fibre size histograms for my-elinated fibres in the motor branch to the EDBwere clearly bimodal, indicating that two popula-tions, one made of large alpha fibres and the otherof small gamma fibres (Fig. 7) were present. Intwo animals (PB and PF) terminal branchesinnervating the interossei and containing respect-ively 37 and 40 large myelinated fibres were sub-tracted from the counts obtained at the ankle.The number of myelinated fibres innervating theEDB was as follows: 130 (PA), 107 (PB), 94 (PD),99 (PE), 76 (PF), 48 (PG).These values were fairly stable from one level

to the next (Fig. 7), and observation was madethat the alpha fibres divided only a few millimetres(usually 5) from the motor point.

Comparison of resultsFigure 8 compares, for each animal, the numberof alpha motor fibres, the mean electrophysiologi-cal motor unit estimate obtained during each re-aording session (black columns), and the averageof all these estimates + one standard deviation(white columns). In four animals (PB, PD, PE,PF), the histological count of alpha motor fibres

fell within the range of the average electrophysio-logical estimates, the mean difference between thetwo sets of values being only 9%. For animal PA,there was a larger discrepancy between the twovalues which could be due to an overestimationof the number of alpha motor fibres innervatingthe EDB, since no search was made for a branchending in the interosseous muscles. In the lastanimal (PG) with L7 ventral root injury, therewere only 48 alpha motor axons innervating theEDB, which is about half the number found inthe others. This was reflected by the electrophysio-logical motor unit estimates obtained throughoutfive recording sessions carried out over a post-operative period of 70 days (Fig. 4). However,during the following 20 days four sessions gavemuch higher values which were about twice theanatomical count.

LEFT (NORMAL) EDB

Electrophysiological estimates of the number ofmotor unitsAn estimate of the number of motor units wasobtained in the left EDB (normal side) in fiveanimals. The average number of motor units (+

MOTOR20 BRANCH TO EDB1 A

A 102 N 137

20]10

E t = 1< j1Fig. 7 Histograms of calibre spectra from the motor0W4L&J 20 branch to EDB at different distances from theaII2 c muscle (A to D) in monkey PE. The two peaks seenl N 137 finhistograms are considered to represent axons ofiE 101 r' _ gamma neurones (first peak) and alpha neurones

'> n _ (second peak, filled), respectively.

V - 7r -

3 5 7 9 11 13 15

DIAMETER (pm)

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150

130'

10'

90

70

50

30-

PA PB PD PE PF

130a...................I.......

PG

...... N. of alpha fibres

99a1 T

Recording sessions

Fig. 8 Estitnated niumbers of motor units in EDB tnuscles of each of thlesix deafferen ted aniimals. Black columns: tnean estitnate obtainied duringeachl recording session; white colutnns: mean numiiber for all sessions ±onestandard deviation (bars). Horizontal hatched lines indicate number of alpliamotor fibres counted in the nerves.

one standard deviation), calculated from 20 deter-minations, was found to be respectively: 121+24(PA), 112+15 (PB), 136+27 (PD). 130+18 (PE),100+9 (PF). These values were higher than on

the right deafferented side (average difference of27%.), and the amplitude of the supramaximalresponses was also greater with an average differ-ence of 36°, between the two sides.

Histological counts of the number of alpha motorfibresFibre size histograms obtained from the motorbranch to the EDB were bimodal with a group oflarge and a group of small myelinated fibres.Subtraction was made in two animals (PB andPF) of the fibres innervating the interosseousmuscles, and the number of large myelinated fibreswas divided by two (Cooper 1966) in order to ob-tain the approximate number of alpha motorfibres. The values were as follows: 168 (PA). 135(PB), 152 (PD), 145 (PE). 165 (PF).

C omparison of resultsIn all animals, the electrophysiological motorunit estimates were lower than the anatomicalcounts (Table 2). In three of them (PB, PD, PE)the difference was minimal (average 12/C). It was

more pronounced in two animals (PA, PF) inwhom one cannot rule out a genuine overestima-tion of the number of alpha motor fibres innervat-ing the EDB. In animal PA no search was madefor a terminal branch ending in the interosseous

Table 2 Left EDB miuscle

Animal Mean numriber of miotor units Number of alpha fibres

PA 121 24 168PB 112-15 135PD 136 + 27 152PE 13018 145PF 100 9 165

muscles whereas in animal PF this branch dividedprofusely but only one fascicle could be dissected.

Discussion

In spite of the ready accessibility of peripheralnerves and muscles to histological and electro-physiological examination, neuromuscular dis-orders are often difficult to diagnose. Nervebiopsies are commonly restricted to a fewcutaneous nerves and can be done only once.Information obtained from muscle biopsies maybe insufficient for diagnostic purposes. Routineelectromyography has also several limitations.For example, there are instances when it cannothelp to decide whether a disease is myogenic orneurogenic in origin since fractionation of motorunits may occur in both conditions, giving rise tothe same pattern of short brief action potentials(Engel, 1975). Above all, none of the conventionalelectrophysiological techniques quantifies thenumber of functioning motor units in a muscle.

Therefore, the motor unit counting techniquedescribed by McComas was considered to be a

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major tool in clinical electromyography. However,the reliability of this method is questionable, con-sidering the wide variability of the motor unitcounts reported in normal subjects (McComas etal., 1971b). Several potential sources of error wereidentified by the authors as explaining this scat-tering of values. One of them recently empha-sised by Brown and Milner-Brown (1976) was thelikely existence of axons with the same thresholdfor electrical activation leading to alternate firingof motor units instead of the expected orderlyrecruitment. They also considered the possibilitythat the 10 or 11 motor units used to calculatethe mean potential amplitude represented an in-adequate sampling of the population of motorunits. With relevance to this hypothesis, motorunits whose action potential voltage was manytimes larger than any of those activated nearmotor threshold have been found in the thenar,first dorsal interosseous, and EDB muscles(Feasby and Brown, 1974; Brown and Milner-Brown, 1976). In patients with muscular dystro-phies, Panayiotopoulos et al. (1974) pointed outanother deficiency of the technique: its inabilityto discriminate small amplitude 'myopathic'potentials close to the instrumental noise level.Ballantyne and Hansen (1974) proposed a com-puterised analysis of the incremental responsesfor a better recognition of motor units but thisapproach is still beyond the reach of mostlaboratories.

Nevertheless, the need to improve the originallydescribed motor unit counting technique dependsvery much on the degree of accuracy of the re-sults it produces. This aspect has so far beenpoorly documented. For this reason, in thepresent study we have compared the electrophysio-logical estimates of the number of motor unitsin the deafferented and normal EDBs of monkeyswith the histological count of alpha motor fibressupplying this muscle, assuming that one motorunit is innervated by one motor axon (Brown andMatthews, 1960; Buchthal, 1960; McPhedran etal., 1965).

After dorsal root ganglionectomy, histologicalstudies confirmed that there were no residual largeafferent nerve fibres in the distal portion of thelower limb. In all cases, the curve of distributionof diameter for myelinated fibres in the motorbranch to the EDB was clearly bimodal, with asharp demarcation between small and large my-elinated fibres, the latter being considered as alphamotor axons. Needless to say, these values do notrepresent the exact number of motor axons exist-ing in an intact nerve since the surgical dorsalroot ganglionectomy implies partial damage to

the motor root fibres (Boyd and Davey, 1966;Gilliatt, 1966; McLeod and Wray, 1967; Wray,1969). Although there was histological evidenceof severe injury to a ventral root supplying theEDB in only one animal (PG), for the otherspartial damage to the motor innervation of theEDB may explain why on the operated side wefound on average a 36% reduction in the ampli-tude of the supramaximal responses and a 27%diminution in the electrophysiological estimatescompared to the normal side.Axonal branching is another factor worth con-

sidering since it is a potential source of errorwhen using anatomical criteria to determine thenumber of motor units in a given muscle. Ecclesand Sherrington (1930) and Wray (1969) havedocumented that it increases with proximity tothe muscle. In our study serial counts of largemyelinated fibres in the deep peroneal nerve atthe ankle remained fairly stable over distances upto 30 millimetres. Division was observed only ata few millimetres (approximately 5) from entryinto the muscle. This, of course, does not excludethe possibility of a division at a site proximal tothe ankle. If so, when reaching this level, thedivided fibres would fall into the group of eitherlarge or small myelinated fibres. In the first case,at the level of the ankle where the stimulationwas applied, they would probably behave electro-physiologically as independent axons even thoughinnervating only part of a motor unit. In the secondcase one would expect the anatomical counts tobe much lower than the electrophysiological re-sults. This was not the case. In four animals (PB,PD, PE, PF) the electrophysiological estimates ofthe number of motor units tended to be lowerthan the anatomical counts. However, the dis-crepancy between the two sets of values was rela-tively small, the overall mean electrophysiologicalestimate being only 9% inferior to the anatomicalcount. In the first animal (PA), there was a largedifference which could be due to an overestima-tion of the number of motor axons supplying theEDB, since in that particular animal no searchwas made for a terminal branch ending in theinterosseous muscles.The last animal (PG) presents a special interest

since it is the only one in which histological evi-dence was found of a severe injury to a ventralroot (L7) innervating the EDB. In this animala satisfactory correlation was observed betweenanatomical and electrophysiological data duringthe first 70 days after the operation. During thelast 20 days, there was a marked increase of theelectrophysiological estimates reaching values ofabout twice the anatomical count of motor axons.

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To explain this finding it is proposed that duringthis second period a reorganisation of motor unitwas taking place through collateral sprouting. Insuch a situation, precarious transmission in certainnewly-formed neuromuscular junctions (Stalbergand Ekstedt, 1973) could produce motor unitpotentials of variable voltage and which couldchange from one stimulation to the next givingrise to 'false' increments. If so, the technique ofMcComas, which relies on the stability of the in-cremental responses, could be inapplicable atcertain stages in case of partial denervation.On the non-deafferented side, the approximate

number of alpha motor axons supplying the EDBwas obtained by dividing by two the population oflarge myelinated fibres in the motor branch of thedeep peroneal nerve at the ankle. With thiscriterion mentioned by Cooper (1966) a good cor-relation between electrophysiological and ana-tomical counts of motor units has been found inthe EDB muscle of man (McComas et al., 1971b),and in the soleus of rat (Eisen et al., 1974). In ourstudy, in three animals (PB, PD, PE) there was aclose anatomophysiological correlation, theelectrophysiological estimates being on averageonly 12% inferior to the anatomical determina-tions. The other two animals (PA and PF) showedlarger differences with estimates respectively 39%and 28% inferior to the anatomical counts. Asmentioned earlier there is reason to believe that,in these animals, the anatomical count was over-estimated and included motor axons innervatingthe interosseous muscles.

In conclusion, in normal and deafferented EDBsof monkeys a satisfactory correlation was observedbetween anatomical and electrophysiological esti-mates of the number of motor units using thetechnique of McComas. However, the discrep-ancy between the values noted in one animal witha severe lesion of the motor innervation of theEDB raises doubts about the reliability of thetechnique in some cases of partial denervation.

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Electrophysiological of motor monkey extensor digitorumUniversitg de Montreal, Montreal, Que'bec, Canada SUMMARY The electrophysiological technique used to estimate the number of motor