Journal ofNeurology, Neurosurgery, and Psychiatry 1984;47:1102-1108

Neurophysiological changes following traumaticspinal lesions in manS TAYLOR, P ASHBY, M VERRIER

From the Lyndhurst Hospital, and Playfair Neuroscience Unit, Toronto Western Hospital, Toronto, Canada

SUMMARY Neurophysiological observations were made on normal subjects and on 57 patientswho had had injuries to the spinal cord. The amplitude of the muscle compound action potential(M response) recorded from triceps surae in response to supramaximal stimulation of the tibialnerve was reduced in the patients indicating that there are changes in motor units below the levelof a spinal lesion in man. In the patients who were clinically spastic it was found that: (1) Theproportion of the triceps surae motoneuron pool reflexly activated either by tapping the Achillestendon or by stimulating the tibial nerve just below the threshold of the alpha motoneuron axons(H reflex) was greater than in normal subjects. This can be explained by an increase in theexcitability of central reflex pathways. (2) Vibration of the tendo Achilles depressed the H reflexless effectively than in normal subjects. This may indicate altered transmission in the pre-motoneuronal portion of the H reflex pathway. (3) The H reflex elicited 50 and 100 ms after astandardised conditioning stimulus to the tibial nerve and expressed as percentage of the uncon-ditioned reflex was greater than in normal subjects. This could reflect a change in the excitabilityof motoneurons or of interneurons.

Spasticity can be defined as "a motor disordercharacterised by a velocity-dependent increase intonic stretch reflexes (muscle tone) with exaggeratedtendon jerks".' The neurophysiological basis for thisclinical syndrome is unknown. Most observations onspasticity have been made on mixed groups ofpatients with cerebral, spinal and diffuse lesions27although there is no reason to expect that identicalneurophysiological abnormalities will result fromsuch anatomically diverse lesions. The simplest formof spasticity is likely to be that resulting from spinaltransection, but as yet there are little firm data onthe neurophysiological abnormalities in patientswith purely spinal lesions.8'2 For this reason, wemade recordings on a coherent group of patientswith spinal cord injuries to determine whichneurophysiological abnormalities were associatedwith spasticity of spinal origin.

Methods

SubjectsPatients with traumatic spinal cord lesions undergoingAddress for reprint requests: Dr P Ashby, Ste. 203, 25 LeonardAve., Toronto, Ontario, M5T 2R2 Canada.

Received 11 November 1983 and in revised form 29 March 1984.Accepted 1 April 1984

rehabilitation at a regional spinal injury centre wereexamined after obtaining informed consent. Clinical andneurophysiological observations were made at threestages: on admission (usually 1 month after injury), 4months after admission, and just prior to discharge. Therewere six female and 51 male patients aged between 17 and77 yr (mean 32 yr). Normal data were obtained from 21normal subjects-10 female, 11 male aged between 19 and42 yr (mean 29 yr).

Clinical assessmentA clinical assessment was carried out just before theneurophysiological testing. Patients were classified as"flaccid" if (1) their lower extremities could be movedpassively (both slowly and rapidly) without eliciting anystretch reflex as detected by an increase in resistance topassive movement or a visible contraction of the stretchedmuscle and (2) the tendon jerks in their lower limbs wereeither absent of diminished, or "spastic" if (1) there wassignificant resistance to passive movement of the lowerlimbs accompanied by a visible muscle contraction whichcould be obtained on, at least, five successive stretches and(2) the tendon jerks in their lower extremities were exagg-ei ated. Patients who did not fall clearly into either of thesegroups were classified as "intermediate."

Neurophysiological examinationSubjects lay prone with the leg to be examined immobil-ised in a padded frame with the knee extended and the

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Neurophysiological changes following traumatic spinal lesions in man

ankle fixed at 900. Compound muscle action potentials oftriceps surae were recorded with surface electrodes. Theactive electrode was placed over the soleus muscle justdistal to the tendinous insertions of the gastrocnemii. Theindifferent electrode was placed 8 cm distally over thetendo Achilles and the ground was placed over the uppercalf. The evoked muscle responses were amplified usingstandard electromyographic differential amplifiers (gain200 to 2000 times) with band pass 10 Hz to 30 kHz. Thepeak to peak amplitudes of the muscle compound actionpotentials were measured from polaroid photographs. Theduration of the negative (upward) peak was measuredfrom the first deflection from the base line to the end of thenegative phase.The outputs of a Medical Systems Corporation dual high

voltage stimulator (type 3072) were linked so that stimuliof different voltages could be delivered through the samebipolar electrode at selected intervals. The linkage did notsignificantly affect the delivered current from eitherstimulator at the settings used. The timing of the stimuliwas controlled by a Digitimer 4030. The reflex (H reflex)and direct muscle (M response) responses were elicitedusing square wave stimuli, 0-5 ms duration, applied overthe tibial nerve in the popliteal fossa. The position of thebipolar stimulating electrode was systematically adjustedin an attempt to obtain the H reflex at the lowest possiblethreshold and without any direct muscle response in thesoleus or gastrocnemius muscles. The electrode was thenimmobilised by means of a rubber strap. The Achilles ten-don reflex (T reflex) was elicited by supramaximal mechan-ical stimulation of the tendo Achilles using a manual ham-mer fitted with a switch which triggered the oscilloscope oncontact. Vibration was applied to the tendo Achilles usinga Wahl vibrator (frequency 60 Hz, undamped amplitude1 5 mm).

Procedure(a) H-M recruitment curve with and without vibration. Thedata for two complete H-M recruitment curves (one withand one without vibration) were collected in the followingmanner. The stimulus current was increased in smallincrements until it was supramaximal for the M response.After a control H reflex was obtained at each stimuluslevel, the vibrator was applied to the tendo Achilles for 20seconds and the stimulus repeated during continuous vib-ration. A period of 90 seconds then elapsed before the netcontrol response was elicited to avoid any delayed effectsthat could result from vibration.

(b) H reflex conditioned by stimulus that just failed to excitemotor axons. Two stimulators were now connected so thatpaired stimuli of different strengths could be delivered tothe tibial nerve through the same electrode. The condition-ing stimulus was set just below the threshold of the motoraxons in the tibial nerve. This was established by inspectionof the calf muscles and the EMG trace on the storageoscilloscope and was monitored during the experiment. Anincrease in the delivered current could be detected by theappearance of the M response and a decrease by a reduc-tion in the reflex response. The intention was to deliver aconditioning stimulus exciting as similar a proportion ofthe large muscle afferents as possible in every subject. The

reflex response (Hs) to this standardised conditioningstimulus was recorded.

Trials were made every 30 seconds. The test stimuluswas given alone (the control situation) or was preceded bya conditioning stimulus either 50 or 100 ms earlier. Thetest stimulus was increased in increments until the data forthree complete H-M recruitment curves (unconditionedcontrol, condition-test interval 50 ms and condition-testinterval 100 ms) were obtained. The maximum con-ditioned H reflexes were then expressed as a percentage ofthe maximum unconditioned reflex.

(c) H reflex conditioned by an afferent volley that was justsubthreshold for an H reflex. The conditioning stimulus wasnow reduced until it just failed to produce an H reflex.Clearly if we reduced the stimulus too much we mightexcite no afferents at all. To avoid this we chose a stimuluslevel which (1) produced no H reflex with the subject atrest and (2) resulted in the reflex activation of a few motorunits if the stimulus was slightly increased or if, wherepossible, the subject made a voluntary contraction of sol-eus. We also recorded whether (1) a small H reflex hadoccurred at any time during the study (as a result of spon-taneous variations in the excitability of the motoneuronepool) or (2) the conditioning stimulus ever modified theresponse to the test volley (for example when the teststimulus and resulting H reflex were small). In mostinstances this documentation provided indirect evidencethat the conditioning stimulus was not below the thresholdof all the sensory nerve axons.

Trials were made every 30 seconds. The test stimuluswas given alone (control situation), or was preceded by aconditioning stimulus 50 or 100 ms earlier. The teststimulus was increased in small increments until the datafor three complete H-M recruitment curves were collectedthe same way as before. The maximum conditioned Hreflexes were expressed as a percentage of the maximumcontrol H reflex.

(d) Achilles tendon reflex (T reflex). The response to threesupramaximal reflex hammer blows to the Achilles tendon5 seconds apart were recorded and their peak to peak amp-litudes averaged.

Statistical analysisThe clinical and neurophysiological data were stored oncomputer files and analysed using standard statistical pro-cedures including one-way and two-way analysis of var-iance and Tukey multiple range tests, Chi-square, t testsand Pearson correlation coefficients. Probabilities (twotailed) of less than 0-05 were considered significant.

Results

In all, 104 successful studies were carried out onpatients, 61 were on quadriplegics (29 with clinicallycomplete and 32 with incomplete lesions) and 43 onparaplegics (29 clinically complete and 14 incom-plete). The studies were made at intervals varyingfrom 1 to 28 months after the spinal cord injury.

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Table 1 Neurophysiological data from normal subjects and patients with traumatic spinal cord injuries classified onclinical grounds as "flaccid", "intermediate", or "spastic". Number ofobservations in brackets. An asterisk indicates asignificant difference (p < 0-05) from the normal data in the top row. An estimate of the area of the compound actionpotential recorded with surface electrodes over the soleus muscle in response to supramaximal stimulation ofthe tibial nerve("M area") is reduced in all three ofthe patient groups. In patients classified as spastic the proportion ofthe triceps suraemotoneuron pool activated by a tendon tap (T reflexlM%)o is greater, but the maximum H reflex Mmax% is not significantlydifferent than normal. There is less suppression of the H reflex by vibration (HvibIH%lo) in patients with spasticity.

M Area (units) T reflexIM % Hmax%IM HviblH%

Normal subjects 117 26 61 25(20) (21) (21) (21)

Patients with cord lesions Flaccid 53* 28 50 36(26) (27) (27) (21)

Intermediate 69* 30 50 43(31) (33) (33) (29)

Spastic 73* 47* 70 61*(38) (39) (39) (38)

The M responseThe peak to peak amplitude of the M response wassignificantly smaller in each of the patient groupsthan in normal subjects. To exclude the possibilitythat this was due to dispersion of the compoundaction potential (the duration of the negative peakwas slightly longer in patients) an estimate of thearea was calculated by multiplying the peak to peakamplitude by the duration of the negative peak. This"M area", which was expressed in arbitrary units,was also significantly smaller in each of the patientgroups than in the normal subjects (p < 0 05) (fig 1,table 1). The reduction in "M area" was observed asearly as 1 month after the lesion. The "M area" wassmaller in those with complete spinal lesions (mean54 "units") than in those with incomplete lesions(mean 81 "units") (p < 0.05).

T refiexIM ratioThe proportion of the motoneuron pool of tricepssurae activated by an Achilles tendon tap (the T

200-

0-

2 100-

1.

N F I S

Fig 1 Maximum compound action potentials of tricepssurae in normal subjects (N) and in patients with spinallesions who were clinically flaccid (F), intermediate (I) or

spastic (S). The means and standard deviations ofestimates(see text) ofthe areas ofthe compound action potentials are

shown. The means for each of the patient groups are

significantly smaller thani the mean for the normal subjects.

reflex/M ratio) was significantly greater in the spasticgroup (p < 0.05) than in all other groups (table 1).Within the spastic group this ratio was greater inpatients with incomplete lesions than those withcomplete lesions (p < 0.05). The ratio increasedwith increasing duration of the lesion for all groups(r = 0-38; p < 0.001).HmaxIM and HsIM ratiosThe largest proportion of the triceps suraemotoneuron pool that could be reflexly activated(the maximum H/M ratio) was not significantly dif-ferent from normal in any of the patient groups(table 1). However, when a "standard" afferent vol-ley (elicited by stimulating the tibial nerve just

1001

Normal Spastic(n=21) (n=31)

Fig 2 The proportion ofthe triceps surae motoneuron poolexcited by a stimulus to the tibial nerve (just below thethreshold of the alphamotoneuron axons) is significantlylarger in patients with spinal spasticity than in normalsubjects. Means and standard deviations shown.

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Neurophysiological changes following traumatic spinal lesions in manTable 2 Data from conditioning studies in normal subjects and patients with traumatic spinal cord lesions. Number ofobservations in brackets. An asterisk indicates a significant difference (p < 0.05) from the normal data in the top row. Usinga conditioning stimulus which was just below the threshold from the alpha motoneuron axons (but suprathreshold for theHreflex) the testH reflex was greater in the patients classified as "intermediate" or "spastic" at both the 50 and 100 mscondition test intervals. When the conditioning stimulus was just subthreshold for an H reflex there were no significantdifferences in the recovery ofthe test H reflex between normal subjects and patients.

Suprathreshold conditioning Subthreshold conditoningH 50/H % H IOOIH % H 501H % H IOOIH %

Normal subjects 39 58 93 94(21) (21) (21) (21)Patients with cord lesions Flaccid 61 77 101 102(14) (14) (13) (13)Intermediate 68* 85* 98 99(19) (19) (20) (20)Spastic 59* 91* 98 98(31) (31) (29) (28)

below the threshold of the alpha motoneuron axons)was used a greater proportion of the triceps suraemotoneuron pool was excited in patients with spas-ticity (64%) than in normal subjects (43%; p <0-01) (fig 2).

H-vibIH control ratioThe ratio of the maximum H reflex during vibrationto the maximum control H reflex (Hvib/H controlratio) was greater in the spastic group than in thenormal or the other patient groups (p < 0-05) indi-cating that vibration was less effective in suppressingthe H reflex in the spastic patients (table 1).TheHvib/H ratio increased with the duration of the

T- -*~~~~l ;T ,I I

-I

u Ar

50 100(ms)

Fig 3 Recovery ofthe H reflex in normal subjects (solidlines) and patients with spinal spasticity (dashed line). Whenthe conditioning stimulus is just below the threshold ofthealphamotoneuron axons but sufficient to excite themotoneurons reflexly (flled squares) the recovery is faster inthe patients with spasticity. When the conditioning stimulusis below the threshold for an H reflex (filled circles) there isno significant difference between the two groups. Means andstandard deviations shown.

lesion for all patients (r = 0*27; p < 0-001), but wasunrelated to the level of the lesion or to whether thelesion was complete or incomplete.Conditioned H reflexSatisfactory conditioning studies were completed on64 occasions. When the conditioning stimulus wasjust below the threshold of alpha motoneuronaxons, the maximum H test/H control ratio 50 and100 ms later was greater in the patients with spastic-ity (and in the intermediate group) than in normalsubjects (table 2). These ratios showed a weak posi-tive correlation with duration of lesion. When theconditioning stimulus was just subthreshold for theproduction of an H reflex, however, there were nodifferences between the normal subjects andpatients (fig 3, table 2).The first type of conditioning volley used results in

an H reflex. Does the muscle contraction producedby this conditioning volley influence the H reflexrecovery curve? In separate experiments on tennormal subjects we conditioned the H reflex with amuscle contraction produced by stimulating thetriceps surae directly. There was no significant alter-ation in the test H reflex amplitude until theconditioning-test interval was greater than 70 ms.The H reflex was then depressed. It thus appearsthat the afferent barrage resulting from a previousmuscle contraction has no influence on the H reflexat the 50 ms condition-test interval although it couldcontribute to the depression of the H reflex at the100 ms interval.

Discussion

The muscle compound action potentialThe maximum muscle compound action potentialswere smaller in the patients with spinal lesions espe-

100

Ht,Hc

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cially when the spinal lesion was clinically complete.This has been noted before in triceps surae8 and in asmall muscle of the foot.'3 The reduced electricalsignal may be partly due to the disuse atrophy ofmuscle fibres which follows upper motor neuronlesions'4-'6 but motor unit counts have shown areduction in the number of functioning motor unitsin muscles below a spinal lesion in man.'7

Tendon jerk and H reflexThe proportion of the triceps surae motoneuronpool activated by an Achilles tendon tap (T reflex/Mratio) was increased in the patients with spasticitybut the largest proportion of this motoneuron poolwhich could be reflexly activated electrically(Hmax/M ratio) was not. This situation has beendescribed in spasticity from mixed and cerebrallesions5-'8 with the suggestion that the dispropor-tionate increase in the tendon jerk might reflect achange in spindle excitability. However, we foundthat a standardised electrical stimulus to the tibialnerve (just below the threshold of the alphamotoneuron axons) also reflexly activated a largerproportion of the triceps motoneuron pool inpatients with spasticity than in normal subjects. Onepossible explanation for these findings is that inspasticity there is an increase in the excitability ofwhatever central pathways are common to the ten-don jerk and the H reflex, but that the maximum Hreflex normally excites such a large proportion of themotoneuron pool that little further increase is poss-ible. An increase in central excitability could resultfrom alterations in the properties of the presynapticpathway, the ease of which motoneurons arerecruited or the state of interneurons capable ofinfluencing motoneurons. We now tried to distingu-ish between these possibilities.

Suppression of the H reflex by vibrationIn normal subjects vibration of a limb causes a strik-ing depression of the H reflex.'9-2' The depressionoccurs some time after the onset of vibration andmay outlast the vibration by several hundred ms,22so it is unlikely to be due to occlusion in the afferentnerve fibres (the "busy line" effect). Vibration alsosuppresses the facilitation of single motors unit bygroup 1 volleys without changing the motor unitsfiring rate (and, by implication, its excitability).23 Ifthe H reflex is accepted as being largely mediated bya monosynaptic pathway, the locus of the suppres-sive effect of vibration is "premotoneuronal" (forexample, due to presynaptic inhibition, transmitterdepletion of failure of invasion of some afferentterminals).

Vibration produces less depression of the H reflexin patients with spasticity'820 and we confirm that

Taylor, Ashby, Verrierthis is also the case for a large group of patients withspasticity from spinal lesions. Either the mechanismswhich normally block the H reflex (see above) areless effective in spasticity or vibration produces agreater background facilitation of motoneurons inspasticity. The latter explanation is not supported bythe findings of Sommerville and Ashby.23

Conditioning studiesWe explored the excitability of the presynaptic andpostsynaptic segments of the H reflex pathway byusing conditioning volleys that excited themotoneurons and conditioning volleys that justfailed to do so. There are several variables that mustbe controlled in such conditioning experiments. Thestrength of the test stimulus is critical. A small test Hreflex is more affected by conditioning volleys than alarge one.24 25 To overcome this difficulty we plottedthe entire H-M recruitment curve at eachconditioning-test interval and chose only the largestcontrol and conditioned H reflexes.The strength of the conditioning stimulus is also

crucial. The stronger the conditioning stimulus thegreater the inhibition of the H reflex.22426 As this isdue, in part, to inhibitory effects arising from thestronger conditioning volley,27 28, we chose a condi-tioning volley just below the threshold formotoneuron axons in order to excite as similar apopulation of afferents as possible in the normalsubjects and spastic patients. Motor and sensoryconduction velocities do not change in thesepatients'7 so the relative thresholds can be assumedto be similar to those in normal subjects. We foundthat the test H reflex (expressed as a percentage ofcontrol) was larger in spastic patients at intervals of50 ms and 100 ms following such conditioning vol-leys (fig 3). This has also been reported in spasticityfrom cerebral and mixed lesions.2 34 7 29 The refrac-tory period of afferent nerve fibres is known to bevery short and can be neglected as contributing to Hreflex depression. The larger H reflex in spasticpatients following a conditioning volley could resultfrom more rapid recovery of excitability of the pre-synaptic terminals or of the population ofmotoneurons or from changes in the late arrivingsynaptic activity arising from the conditioning volley(or from the consequent muscle contraction).We tested transmission in the presynaptic seg-

ment of the H reflex pathway by conditioning the Hreflex with an electrically induced afferent volleyjust insufficient to excite the motoneurons reflexly,but presumably still sufficient to excite some of thelarge afferents and their presynaptic terminals.There were no significant differences between thenormal subjects and spastic patients. Thus the pre-synaptic changes produced by a single volley are

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Neurophysiological changes following traumatic spinal lesions in man

inadequate to explain the observed changes in Hreflex recovery cycle, even though conditioning withmultiple mechanically induced afferent volleys (vib-ration) appears to reveal changes in presynaptictransmission in spasticity. The faster recovery of theH reflex in the spastic patients must be explainedeither by increased excitability of motoneurons orby changes in late arriving synaptic activity resultingfrom the conditioning volley. We cannot distinguishbetween these possibilities in the present study.

Teasdall et aP° observed late responses to musclestretch in the chronic hemisected cat implyingaltered excitability in interneuronal pathways andDimitrijevic and Nathan" reported prolongation ofthe action potential resulting from a tendon tap. Forthis reason, we looked carefully at the action poten-tials resulting from tendon taps in our patients.There were no late inflections or waves following themain complex to suggest polysynaptic activation ofmotoneurons.Could any of the present findings be explained by

an alteration in the motor units of triceps surae? Forexample, if there was a selective atrophy of type II,phosphorylase rich, muscle fibres-which has beendescribed in spasticity following hemispherelesions,'8 although not consistently following spinallesions in man'4 31 or animals,32 33 theneurophysiological properties of motor units inner-vating type I fibres might dominate the recordings.Motoneurons innervating slow twitch fibres havehigher input resistances and larger EPSPs.34 Theirpredominance in spastic patients could account for ahigher T reflex/M ratio. However, thesemotoneurons have longer afterhyperpolarisation34and this would tend to delay the recovery of the Hreflex following a conditioning volley. Thus, a selec-tive loss of a population of motoneurons or atrophyof their muscle fibres cannot provide a satisfactoryexplanation for all the present findings.

We thank the Physician's Services Incorporated, theMultiple Sclerosis Society of Canada, and the Medi-cal Research Council of Canada for financial sup-port, the physicians of Lyndhurst Hospital for theircooperation, the Health Care Unit, University ofToronto for statistical analyses.

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in man.following traumatic spinal lesions Neurophysiological changes

S Taylor, P Ashby and M Verrier

doi: 10.1136/jnnp.47.10.11021984 47: 1102-1108 J Neurol Neurosurg Psychiatry

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