Acta neurol. scandinav. 57, 329-344, 1978

Department of Neurology, Medical School Hospital, Aegean University, Bornova, Izmir, Turkey

Evoked electrospinogram in spinal cord and peripheral nerve disorders

CWHUR ERTEKIN

Spinal cord evoked potentials have been studied by means of intrathecal application in 80 patients with various spinal cord and peripheral nerve disorders.

neuropathy, generalized anterior horn cell disease and in discrete lesions of dorso-lumbar segments. On the other hand, the first component of the segmental response is delayed, reduced and sometimes dispersed or lost in chronic sensory-motor polyneuropathy and in hereditary spinocerebellar degeneration. The reduction in amplitude is also present in multiple scle- rosis with clinical signs of dorsal funiculus involvement.

In compressive lesions of the cauda-conus, recordings of lower thoracic intervertebral level show that the segmental responses are delayed with marked amplitude reduction.

The potentials recorded from lumbo-sacral segments show a greater amplitude of the second component proportionally to the first one as the duration of second component is longer in spastic paraplegia regardless of its etiology.

The cervical tractus response is seen to be markedly slowed with a re- duction of amplitude or is often absent in chronic polyneuropathy, spino- cerebellar degeneration and in multiple sclerosis.

The primary sensory neurones lying both in periphery and in the dorsal column are assumed to be responsible for the segmental evoked potentials especially for the first component. The late slow component is related to the activation of interneurones situated within the segmental gray matter and segmental collaterals of the dorsal root fibres carrying impulses to those cells. Cervical tractus responses are mostly formed by the dorsal column fibres and their physiological action upon demyelination is similar to that of the peripheral nerves.

The segmental spinal cord potentials are normal in acute motor poly-

A segmental spinal cord potential is obtained from the intrathecal electrode when a needle recording electrode is introduced into the subarachnoidal space around the midline, and the major peripheral nerves related to the spinal segment in question is stimulated supramaximally.

The segmental responses recorded in this situation are composed of a fast early and a slow late components. This is called a CD potential and its first

22 Acta neurol. scandinav. 57:4

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component is shown to be related to the activity of the ascending dorsal funiculus fibres. The late slow component of the segmental evoked potential is thought to be related to the pre- and postsynaptic activity of the hori- sontally oriented fibres within the segmental gray matter (Ertekin 1976a).

If the electrode is behind the cord dorsum at the lower cervical level, it is easily possible to obtain a triphasic compound action potential on stimulation of the leg nerves. The “Tractus potential” has been found to be originated mainly from the dorsal funiculus fibres (Ertekin 1976b).

In this paper, spinal cord evoked potentials are investigated in the patients with well-known cord disorders or peripheral nerve involvements. Hence, anatomical substracts necessary for the evoked spinal cord potentials could also be explored by a clinico-physiological approach.

MATERIAL AND METHODS

A total of 80 patients (17 females and 63 males) were investigated. All of them were selected from in-patients in the department of Neurology. The ethical principles of the Decleration of Helsinki concerning human experimentation were followed throughout the study. The neurological examination was carried out by the author and two other neurologists. The clinical evaluation of the patients has been completed by means of spine X-rays, myelography, EMG, nerve conduction studies and other routine bio- chemical investigations.

The intrathecal recording technique used in this study was described earlier (Ertekin 1973, 1976a, b). For the recording of segmental cord potentials; the posterior tibial nerve at the popliteal fossa and the median nerve at the elbow were chosen and stimu- lated supramaximally. Subsequent responses were taken from the C 5-6 or C 6-7 intervertebral (1.V.) levels and Th 10-11 or Th 11-12 I.V. levels. The posterior tibial nerve was stimulated in order to obtain cervical tractus potentials from the lower cervi- cal I.V. level. During the recordings of cervical and lower thoracic I.V. levels; while giving very weak electrical shocks from an intrathecal electrode, the recording was done by the other and vice versa. Thus the so-called “intraspinal evoked potentials” were also evaluated in some patients (Erlekin 1976b).

The computer averaging technique was used in order to obtain the very small evoked potentials in the majority of cases (47 patients of the total). For this purpose, the output of the EMG (DISA 14 A 30) amplifier is connected into a UNIMAC-4000 computer for summation. A-D conversion of the computer has a 7-bit resolution with a minimum sampling interval of 10 microsecondsample for the single channel mode and of 20 microsecondsample for two channels simultaneous averaging which was the mode generally used for two I.V. level recording during stimulation of the leg nerve. Computer analysis time was often 75-100 msec but 25-150 msec times were also used when required. In most cases, 128-256 segmental responses were averaged but the summation was increased to 1024 responses in some cases. For cervical tractus poten- tials; 512-1024 responses were preferred for a better resolution. The averaged responses were recorded by a Polaroid camera or on a strip chart recorder. The individual and statistical results have been compared with those obtained from 39 normal subjects published previously (Ertekin 1976a, b).

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Table 1 . Grouping of the patients investigated

A) Diffuse but systematic involvement of the spinal cord or peripheral nerves:

Polyneuropathy . . . . . . . . . . . . . . . . . . . . . . . . . . . 1) Chronic mixed or prominently sensory polyneuropathy

2) Acute motor polyneuropathy (6 cases) Hereditary Spino-Cerebellar degeneration . . . . . . . . . . . . Diffuse anterior horn cell disease 1) Kugelberg-Welander disease (3 cases) 2) Sporadic A.L.S. (3 cases)

(7 cases)

. . . . . . . . . . . . . . .

B) Localized-segmental spinal cord involvement: a) Spinal cord a n d o r root traumatic injuries . . . . . . . . . b) Spinal cordcauda equina compression . . . . . . . . . . . . c) Sequalae of inflammatory lesions (i.e. transversus

myelopathy) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

C) Disseminated irregular involvement of the spinal cord (i.e. multiple sclerosis) . . . . . . . . . . . . . . . . . . . . . . . . . . .

13

8 6

5 14

12

22

80 cases

RESULTS

The patients have been classified into different groups and subgroups as listed in Table 1, according to the well-known and certain anatomical in- volvements judged from their clinical pictures.

Diffuse but systemic involvement of the spinal cord and peripheral nerves

Twenty-seven cases have been investigated under this heading and also divi- ded into three subgroups to clarify the origin of the evoked spinal cord potentials.

Polyneuropathy . Seven of 13 patients with polyneuropathy had chronic pro- gressive course with very marked slowing in sensory and motor nerve con- duction velocities. The remaining six patients showed typical clinical features of acute motor polyneuropathy of Guillain-Barr6 type. These cases were in- cluded into the study during the first month of their illnesses. There was no evidence of primary sensory neurone involvement on the basis of clinical and electrophysiological findings in all but one.

22*

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Hereditary Spino-cerebellar Degeneration. Eight cases were investigated. Four of them had a clinical picture of Friedreich ataxia. In another three patients, pyramidal and cerebellar syndromes were prominent besides the

Figure 1. Lumbosacral spinal cord potentials recorded from Th. 11-12 I.V. level evoked by stimulation of the tibia1 nerve at the right and left popliteal fossa separately. Above: Friedreich ataxia. Middle: Hereditary polyneuropathy. Below: normal control. Twenty superimposed sweeps. Calibration: 40 microvolt, 25 msec. The dotted areas above were

the site of involvement in spinocerebellar ataxia and sensory neuropathies.

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clinical signs of the dorsal funiculus involvement. Only one case displayed features resembling the X-linked hereditary spastic paraparesis without any signs of dorsal funiculus involvement. Median and sural nerve sensory action potentials were either not present or showed very marked amplitude reduc- tion in all these cases except the one with hereditary spastic paraparesis.

DifJuse Anterior Horn CeZZ Diseases. Three cases of Kugelberg-Welander and three cases of sporadic motor neurone diseases were investigated in this group. The clinical pictures were considerably progressed with moderate to severe atrophies in their proximal/distal muscles in all cases.

The segmental evoked potentials from the lower cervical and lower thoracic I.V. levels were either lost or their amplitudes were very small in patients with chronic polyneuropathy and spino-cerebellar degeneration (Figure 1). It has been difficult to obtain the first fast component of the segmental response with the conventional methods or the whole series of potentials have been absent. Therefore the computer averaging was needed. When the averaged segmental responses were discernible, then the onset and peak latencies were either within the normal limits or moderately delayed as in the cases of spino-cerebellar degeneration; or the first component of the segmental re-

Figure 2. Lumbosacral spinal cord potential from a case of chronic sensory-motor polyneuropathy. Stimulation: posterior tibia1 nerve at the popliteal fossa. Recording site:

Th 11-12. I.V. level. 1024 responses. Calibration: 1.0 microvolt, 5.2 msec.

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sponse appeared polyphasic in shape and the onset latency was considerably delayed as observed in chronic polyneuropathy (Figure 2). On the other hand, the segmental cord potentials were found to be normal in all respects in patients with acute motor polyneuropathy (except in one), generalised an- terior horn disease and in a case of hereditary spastic paraparesis.

We failed to obtain cervical tractus responses regularly from the intrathecal erectrode at the lower cervical I.V. level by stimulating the posterior tibial nerve supramaximally. However a very prolonged cervical tractus response was just discernible in a case with chronic polyneuropathy and a case with Friedreich ataxia (Figure 3). The cervical tractus response was found to be normal in acute motor polyneuropathy and in generalised anterior horn cell disease, although its amplitude was somewhat reduced in later cases.

The very slow and delayed “Intraspinal evoked potentials” could be evoked by stimulation of the lower cervical cord during the lumbo-sacral

t 1 I I I I 1

25 100 SO 75 0 m Sec

Figure 3. Cervical tractus potentials recorded from C 6-7 I.V. level evoked by stimula- tion of the tibial nerve at the popliteal fossa. Above: Guillain-BarrC syndrome. Middle: Chronic sensory-motor polyneuropathy. Below: Friedreich ataxia. 512 (above) and

1024 (middle and below) responses.

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recording in two cases of chronic polyneuropathy and in one case of spino- cerebellar degeneration. The conduction velocities of these potentials along the spinal cord were slow and between 5-8 m/sec (Figure 4).

Figure 4. “Intraspinal Cord Potentials” evoked by stimulation of cervical cord at the C 6-7 I.V. level and recorded from the T h 11-12 level. Single oscilloscopic traces. Above: A normal control (stimulation; 1.0 volt and 0.1 msec). Middle: hereditary poly- neuropathy (stimulation; 3.5 volt and 0.1 msec). Below: spino-cerebellar ataxia (stimula- tion; 30 volt and 0.05 msec). Calibration: 25 msec for all and 40 microvolt for above

and middle, 120 microvolt for below.

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Localized-segmental spinal cord involvement

This group includes the patients showing a clinical picture of localized seg- mental involvement somewhere in the long axis of the spinal cord. Thirty-one cases of various etiology have been studied and the lesions have been found in a few segments of the spinal cord or at the cauda equina. The major causes were tumoural compression, cord trauma and the sequelae of transversus myelopathies.

Segmental potentials recorded from far above and far below the discrete lesion were found completely normal (Figure 5 ) and the amplitude reduction was seen to be a main finding in recordings around the site of lesion (Figure 6). Whereas the recording from the lower thoracic I.V. level with compressive lesions of Conus-Cauda (six cases) has shown delayed segmental responses with marked reduction in amplitude (Figure 7). Similarly it was not easy to record any cervical tractus response in the dorso-lumbar spinal lesions. If it was obtainable (as in four cases) there has been a moderate slowing in con- duction along the spinal cord ranging from 22 to 30 Wsec.

Figure 5. Lumbosacral spinal cord potentials recorded from the Th 10-11 1.V. level evoked by stimulation of the tibia1 nerve at the left (above) and right (below) popliteal fosssa. A patient with lower cervical cord compression. 256 responses for each. Calibra-

tion: 5.0 msec and 3.7 microvolt.

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Disseminated-irregular involvement of the spinal cord; multiple sclerosis

All cases in this group have been diagnosed to have multiple sclerosis (M.S.) according to the criteria reported by McAlpine et al. (1965). Sixteen of them showed signs and symptoms of dorsal funiculus involvement while in six, vibration and position senses were found to be normal.

The cervical tractus responses were found to be abnormal in all 14 cases of M.S. having position and vibration sense disturbances. There was no cIinical sign of dorsal funiculus involvement in the remaining six patients but the loss of tractus response or reduction in ampIitude and delaying in latency was found to be present in half of them. As a whole, cervical tractus re- sponses were studied in 20 cases and were found to be absent in 12. The latency of the first positive peak of response was 27.5 msec on the average in eight M.S. cases (ranging from 21 to 52 msec) which was 30 % more prolonged than the normal mean delay of 21 msec (Ertekin 1976b). It was also possible to estimate the conduction velocity along the spinal cord in five cases and found to be 23 WSec on average (range: 16-28 WSec) which was well below the normal limits of 30 WSec of the normal controls and the

Figure 6. Lumbosacral spinal cord potentials recorded from the T h I?-LI I .V. level evoked by stimulation o f the tibia1 nerve at the left (above) and right (below) popliteal fossa. A patient with extramedullary lumbosacral cord compression. 256 (above) and 512 (below) responses. Calibration: 5.0 msec and 1.8 microvolt (above) 0.9 microvolt (below).

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degree of mean reduction in velocity was about 40 % of the control values (Evtekin 1976b) (Figure 8). The main abnormality encountered in the seg- mental responses was reduction in amplitude of the first component and the pathological lumbosacral cord potentials were more frequent (Figure 9).

Table 2 summarizes the results obtained from different groups of spinal cord and peripheral nerve disorders.

The late component in spastic paraparesis

An interesting point has been observed in patients with spastic paraparesis when recording is made from the lower thoracic I.V. levels. This is the in- crease in the size of the second component in proportion to the first compo- nent. A graphical illustration of this is given in Figure 10 which has been obtained from 21 controls and 16 spastic cases. If the amplitude and duration of the first component is assumed 100, the amplitude of the second com- ponent is 88 on average and the duration is 248 in normal controls. In patients with spastic paraparesis, the amplitude of the second component has been higher (179.5 % of the first component) and the duration of the second component has been longer (350 % of the first component on average).

Figure 7 . Lumbosacral spinal cord potentials recorded from Th 11-12 I.V. level evoked by stimulation of fibular nerve at the right capitulum fibulae. A patient with Conus-Cauda compression. 1024 responses. Calibration: 10 msec for above and 5 rnsec

for lower traces, 0.2 microvolt for each.

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Table 2 . Summarizing the results obtained from patients with different spinal cord/peripheral nerve diseases

The features of

segmental responses tractus The features of Main site of

anatomical involvement responses

Groups of diseases

Poly- neuropathy mixedhensow

Poly- neuropathy acute motor

Hereditary spino- cerebellar degeneration

ALS and Kugelberg Welander disease

Localized segmental spinal cord disease

Multiple sclerosis

Peripheral motor and/or sensory nerves

Peripheral andor spinal motor nerves

Spinal ganglia and dorsal funiculus

Diffuse anterior horn cells

A few segmental levels somewhere along the axis of the spinal cord

Disseminated . spinal lesions mainly in the dorsal and lateral funiculus

Especially first compo- Markedly delayed, nent delayed, diminished or absent diminished or absent

Normal Normal

Prominently diminished Absent sometimes delayed or absent

Normal

1) Normal far above and below the injured cord segments

on the segment related with the spinal lesion

3) Delayed, diminished segmental responses in conus-cauda lesions

2 ) Amplitude reduction

Amplitude reductiosn especially in the first component and molstly in lumbosacral cord

Normal

Generally absent in dorsolomber cord lesions; mild or moderate conduction slowing when present

Delayed and diminished response or often absent

DISCUSSION

The present study indicates that the first component of the segmental evoked potentials is in fact related to the activation of he primary sensory neurones and that antidromic activation of the motor nerve fibres do not significantly influence the segmental evoked potentials. Indeed, in cases of severe motor polyneuropathy and diffuse anterior horn cell disease, the segmental poten-

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Figure 8. Cervical tractus potential (above) from C 6-7 and segmental lumbosacral cord potential (below) from T h 10-11 I.V. levels evoked by stimulation of the left tibial nerve. A patient with multiple sclerosis. 1024 responses for each. Calibration: 10 msec

and 1.8. microvolt.

Figure 9. Lumbosacral spinal cord potentials recorded from T h 11-12 level evoked by stimulation of left (above) and right (below) tibial nerves. A case with multiple sclerosis.

128 responses fo r each. Calibration: 10 msec and 1.8 microvolt.

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tials have been found entirely normal in recording obtained from behind cord dorsum. The abolition of the spinal cord responses following in appropriate dorsal root section also supports that the segmental cord level from which the potentials are recorded is sensory in nature and that antidromic discharges in the motor fibres do not contribute significantly to the segmental potential (Happel et al. 1975).

The latency, duration and amplitude of the first fast component of the segmental potential are dependent upon the input produced by the peripheral nerve stimulation on one hand; and the degree of the temporal and spatial dispersion of the afferent input arriving at the recording site on the other. Thus in the patient with polyneuropathy showing a prolonged conduction velocity in sensory nerves, latencies in the segmental responses were remark- ably delayed; while in patient with spino-cerebellar staxia, reduction in the amplitude rather than conduction delay was more prominent in both sensory nerve action potentials and in the first component of the segmental cord potentials. Since the severe conduction slowing in peripheral nerves is en- countered in polyneuropathy displaying demyelination; the small and poly- phasic disperse response evoked from peripheral nerve is compatible with the slowing in different diameter fibres within the A-fibres spectrum (Kaeser 1970, Gilliatt 1973, Buchthal 1973); similar slow conduction with disperse polyphasic shape of the first component of the segmental responses in poly- neuropathy cases indicates that the large and medium size afferent nerve fibre

Figure 10. The graphical representation of the size relationship between first and second components of the lumbosacral cord potentials in normal controls and in patients with spastic paraparesis. The amplitude and duration of the first components are assumed

as 100.

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activation coming from periphery are mainly responsible for the first corn- ponent of the segmental responses.

The reduction in amplitude has also been observed in the first component of the segmental responses without any latency delay in patient with M.S. having the clinical signs of diffuse dorsal funiculus involvement. In other words, in spite of the normal afferent nerve volIey, the first component of the segmental responses could still diminish though not so low a level as that encountered in sensory polyneuropathy and spino-cerebellar degeneration. These findings support that the dorsal funiculus ascending fibres are the main site of the origin of the first component of the segmental response. Thus both peripheral descending and central ascending branches of the primary sensory neurone should be intact in order to obtain normal segmental cord potential.

The first component of the segmental cord potentials were not influenced by lesions localized far above and far below the site of recording. If the pathological process was located arond the segments recorded intrathecally, the main abnormality was the amplitude reduction of the whole component series. This is probably related with either local destruction and/or functional inactivity of related spinal segment; or in cases of extramedullary mass compressing the spinal cord from the posterior aspect which is due to the increase of volume conduction in between the recording site and the active tissue.

The different behavior of the segmental response components recorded from the spinal cord was observed in patients with spastic paraplegia caused by various spinal disorders. This was the increase of the ratio of the second first component sizes especially prominent for the duration of the second component. The increased and prolonged responsiveness to afferent seg- mental input suggests that the hyperexitability of the interneurones is the cause of such proportional augmenting of the second component in spasticity. In other words, the second component is in fact, mostly related with the segmental post-synaptic and perhaps pre-synaptic neural activities. Experi- mental spinal cord section can cause an augmenting of the amplitude of the negative intermediary potential (N-1 deflection) which is similar to the late slow component obtained from man (Ertekin 1976a) and in the decerebrate preparation, another delayed negative deflection often develops as a corn- ponent of the cord dorsum (Lindblom & Ottoson 1953). These experimental findings also grossly correlate with our human data.

In M.S., when the dorsal funiculus was predominantly affected by spinal lesion; it was difficult to obtain any cervical tractus potential by leg nerve stimulation. If the response was available, its onset latency and latency to the first positive peak of the tractus potential was significantly prolonged and its amplitude was reduced. The mean conduction velocity along the dorsal

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funiculus was about 40 % of those of the normal controls. Such a degree of slowing in conduction velocity observed in the M.S. cases is similar to those findings frequently encountered in peripheral nerve conduction in neuro- pathies with segmental demyelination (GiZZiatt 1973). So that the central ascending fibres of the dorsal column seem to react in similar fashion physio- logically to the demyelination in the dorsal funiculus as it occurs frequently in M.S. This electrophysiological finding is also in accord with the results of the experimental demyelination of dorsal column in which the slowing of conduction velocity along the spinal cord was prominent (Mayer 1966, McDonald & Sears 1970). While in the experimental degeneration of the dorsal column, there was no reduction in conduction velocity up to the time of conduction failure (McDonald & Robertson 1972). In the compressive or inflammatory lesions located around the dorsolumbar segments of the cord, the number of patients studied is not sufficient and the existence of hetero- genous etiologies among the patients may prevent the reaching of a precise conclusion for cervical tractus potentials. Yet the subject merits further systematic study especially for spinal cord trauma and compression.

Conus medullaris and Cauda Elquina lesions deserve mention in a different conclusive way. In such patients, recording just above the lesion (i.e. lower thoracic I.V. level) produce very late segmental responses with reduction in amplitude of the first component. It has been demonstrated experimentally that the early spike component of the segmental potential increases pro- gressively in latency beyond and up to the compression site of the dorsal root, and this is due almost entirely to the decreased conduction velocity of the afferent volley in the root (Gelfan & Tarlov 1956). Furthermore, the observations of the very prolonged reflex conduction time in Bulbocavernosus reflex in cauda equina lesions (Ertekin & Reel 1976) is also in accord with the slowed segmental cord potentials obtained in this study. Therefore con- duction in both reflex and sensory fibres of the sacral roots and nerves are remarkably altered in the manner of focal compressive lesions encountered in peripheral entraptement neuropathy (Kaeser 1970).

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Received December 6, 1977 accepted March 2, 1978 Cumhzir Eriekin, M.D.

Department of Neurology Medical School Hospital Aegean University, Bornova Izmir, Turkey