Journal of the Neurological Sciences, 1987, 80:333-342 333 Elsevier

JNS 02865

Cortical evoked potentials and somatosensory perception in chronic spinal cord injury patients Aleksandar Beri6 l, Milan R. Dimitrijevi61 and Ul f Lindblom 2

~ Division of Restorative Neurology and Human Neurobiology, Department of Rehabilitation, Baylor College of Medicine, Houston, TX 77030 (U.S.A.) and 2Department of Neurology, Karolinska Hospital, Stockholm (Sweden)

(Received 28 January, 1987) (Revised, received 15 April, 1987) (Accepted 15 April, 1987)

SUMMARY

The correlation between somatosensory evoked potentials (SEPs) and. sensory perception was studied in 110 patients with traumatic chronic spinal cord lesions. Perception thresholds over the legs for light touch, vibratory sensibility, temperature and thermal pain were tested together with recordings of tibial and peroneal SEPs. Tibial nerve SEPs correlated better with sensory perception than peroneal nerve SEPs. Normal tibial nerve SEPs were not present with absent or trace vibratory sensibility and vice versa. However, we found many exceptions to the correlation between temperature and pain perception and SEPs. Light touch, vibratory sensibility, and SEPs were highly correlated between each other, while temperature and pain perception correlated poorly to these other modalities. This represents an evident segregation of touch perception, vibratory sensibility and SEPs, which are thought to share dorsal columns as a common ascending pathway, and temperature and pain perception known to be related to the spinothalamic system.

Key words: Somatosensory evoked potentials; Sensory perception; Dorsal columns; Spinal cord injury; Quantitative sensory testing

Correspondence to: M.R. Dimitrijevi6, M.D., Division of Restorative Neurology and Human Neurobiology, Baylor College of Medicine, 1333 Moursund, Houston, TX 77030, U.S.A.

0022-510X/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)

334

INTRODUCTION

The relationship between somatosensory perception and evoked potentials is still controversial. Correlation studies of sensory perception and SEPs usually have used inconsistent methodologies on a small number of patients with various underlying disorders (Dorfman et al. 1980; Giblin 1964; Halliday and Wakefield 1963; Halliday 1967; Mastaglia et al. 1978; Stohr et al. 1982). Furthermore, the majority of these techniques were qualitative (Fukushima and Mayanagi 1975; Giblin 1964; Rowed et al. 1978).

Experimental animal studies usually addressed the problem of pathways conveying the SEPs without differentiating the sensory modalities (Cusick et al. 1979; Norrsell 1966; Schramm et al. 1979; Whitehorn et al. 1969), while human studies differentiated modality abnormalities but not the anatomical pathways (Dorfman et al. 1980; Giblin 1964; Halliday and Wakefield 1963; Halliday 1967). Therefore, many conclusions on pathways operating in the human spinal cord were based on deductions from acute lesions in experimental animals.

In our previous study of chronic spinal cord injury patients, we correlated perception of touch, pinprick, and joint position with peroneal and tibial SEPs (Dimitrijevi6 et al. 1983). These patients represented severe, anatomically diffuse spinal cord lesions with a variable pattern of reorganization during recovery. We found a general correlation between sensibility and evoked potentials, but no specific correlation in any of the tested modalities. In this prospective study we have continued our investigation using quantitative techniques to test light touch perception, vibratory sensibility, temperature and pain, including cold, warmth and thermal pain perception, (Fruhstorfer et al. 1976; Goldberg and Lindblom 1979), and compared the results to peroneal and tibial SEPs. Our purpose was to clarify the relationship between different sensory modalities and SEPs in spinal cord dysfunction.

MATERIALS AND METHODS

110 consecutive patients referred for clinical neurophysiological assessment with traumatic lesion of the spinal cord and neurological levels from C-1,2 to T-12 were studied (66 cervical, 44 thoracic). Their ages ranged from 17 to 60 years and the average was 32.5 years. The average time after injury was 47.2 months, and ranged from 6 month to 25 years. 61 patients had no voluntary motor activity below the lesion while 49 remaining patients had some preserved voluntary activity. 41 had been injured in motor vehicle accidents, 9 in motorcycle accidents, 15 gunshot wounds, 15 diving accidents, 14 falls, and 16 other injuries. The patients were without clinical signs of concomitant head injury and were in good general health with no decubiti, bladder, or other infections. Patients with localized lower extremity pressure neuropathies had been excluded on the basis of clinical findings supported with electromyography, sensory nerve action potentials and lumbosacral SEPs. About two-thirds of the patients were

335

on some form of antispastic medication. Twenty neurologically healthy subjects served as the control population for recordings of cortical SEPs.

All the patients were tested in a sound-proof, temperature controlled (22 ° C) room with the patient supine to provide optimal relaxation and concentration during test procedures. Vibratory threshold (VT) measurements were obtained with a vibrameter (Somedic AB Stockholm) which was designed on the method of Goldberg and Lindblom (1979). The probe was placed over the first metatarsal bone or over the anterior surface of the tibia. Constant probe pressure was maintained by monitoring the pressure indicator. The intensity of vibratory stimulus (120Hz) was controlled manually and the peak to peak amplitude of the probe movement was continuously measured by an accelometer and displayed in micrometers. The VT was determined according to the method of limits and three successive measurements of threshold were averaged for each test site. Temperature perception and cold and heat pain perception were tested with a Marstock thermal stimulator (Somedic AB) based on the technique by Fruhstorfer et al. (1976). The thermode stimulating surface consisting of 36 Peltier elements was either warmed or cooled depending on the direction of the applied current. A thermocouple attached to the thermode measured the change in skin temperature. The thermode was placed laterally over the dorsum of the feet, and thresholds for warm, cool, cold pain and heat pain were recorded. Von Frey hairs were applied perpendicular- ly to the skin of the dorsum of the foot and 50~ perception thresholds were recorded as a measure of light touch perception.

Cortical SEPs from tibial and peroneal nerve stimulations were recorded using silver-silver chloride cup electrodes placed over the modified Cz point (1.5 cm behind Cz) referenced to Fz (International 10/20 system). For the tibial nerve, two different intensities of unilateral stimulation at the knee were used. One was sufficient to elicit a maximal H wave, and the other a maximal M wave of the soleus muscle during simultaneous monitoring of soleus muscle activity. For peroneal nerve SEPs, stimula- tion was done behind the capitulum fibulae with an intensity sufficient to elicit a moderate twitch of the innervated muscles. On two separate occasions 128 responses from each site were averaged with analysis time of 160 ms and sampling interval 312/~s. Teca preamplifier-amplifiers (PA 63-AA6MK3) were used with amplification of 50 000. Analog filters were set to 8-1600 Hz. Responses were averaged by a Hewlett Packard 1000 computer system which was also used for permanent storage and analysis.

CRITERIA FOR ANALYSIS

Results of vibratory thresholds, temperature, cold and heat pain thresholds were compared with age-matched standards (Fruhstorfer etal. 1976; Goldberg and Lindblom 1979). Normative values for the tibial nerve SEP P 30 latency were 32.1 ms with a SD of 1.8 ms for a stimulation intensity eliciting a maximal H wave, and 21.8 ms with a SD of 1.8 ms for an intensity eliciting a maximal M wave. The amplitude values were 6.8 #V with a SD of 2.5 #V for an intensity eliciting maximal M wave. Table 1 shows criteria for dividing the results into 4 categories: normal (N), altered (ALT), trace ( + / - ) and absent (AB). We computed correlations between all combinations of pairs

336

TABLE 1

CRITERIA FOR ASSESSMENT OF SOMATOSENSORY FUNCTIONS

1. Vibratory Up to 3 SD NL perception Up to 50/am ALT

Above 50/am + / - Absent AB

2. Touch Up to 0.495 g NL perception 0.495-2.38 g ALT

2.38-9.6 g + / - Above 9.6 g AB

3. Temperature and Warm, cool, cold pain, heat pain - up to 3 SD NL pain perception Warm-cool increased, cold pain altered, warm- ALT

cool absent and heat pain preserved Some heat pain or cold pain + / - Absent AB

4. Cortical SEP Normal, latency up to 2.5 SD Normal Delayed and low amp. or only delayed above Abnormal

3 SD Some response very delayed and low amplitude Trace Absent Absent

o f the following parameters: vibratory perception, touch perception, temperature and pain perception, and SEPs from the same leg, as well as temperature and pain perception

from the contralateral leg. For these computat ions we used 4 x 4 tables according to the criteria shown in Table 1. In addition, two independent subpopulations were also

analyzed. In the first, 40 patients in whom all responses were absent were excluded. Due to the smaller number of observations 3 x 3 tables were used for comparisons. In the

second subpoputation of 52 patients, a comparison of the correlation of the perception o f vibration, touch and temperature and pain with peroneal SEPs and their correlation with tibial SEPs was made. We used a BMDP-84 (Health Science Computing Facility, U C L A sponsored by N I H Grant RR-3) statistical computer package for all the statisti- cal analysis where chi-square values were obtained for all parameters from 4 x 4 or

3 x 3 tables and then converted to Pearson r coefficients. These were tested further for significant differences between each pair of parameters.

RESULTS

The mean and standard deviations for vibratory perception, touch perception by Von Frey hairs, temperature and pain perception, and tibial cortical SEPs showed no significant difference between right and left extremity, thus permitting the analysis of both sides together. The SEPs obtained from an intensity of stimulation eliciting a maximal M wave were usually better def'med and of larger amplitude, and therefore were used for computat ion of correlations. Table 2 shows the correlations between each of the sensory tests and somatosensory evoked potentials. Correlations between all of the

TABLE 2

CORRELATION BETWEEN TIBIAL SEP AND SENSORY F I N D I N G S IN SCI PATIENTS

337

Parameter pair r a n

Vibration - SEP 0.77 219 Vibration - Touch 0.75 146 Vibration - Temperature and pain 0.40 b 213 Touch - SEP 0.82 145 Touch - Temperature and pain 0.49 b 139 Temperature and pain - SEP 0.39 212

a Pearson r correlation coefficients derived from 4 × 4 tables. b Significant decrease in correlation when observations with all absent parameters were excluded

(P < 0.01).

parameter pairs were significant (P < 0.01). However, they were significantly smaller when temperature and pain was one of the parameters (P < 0.01). When we compared the temperature and pain perception with light touch perception, or vibratory per- ception, or tibial SEP from the same leg, as well as from the contralateral leg, the correlations of temperature and pain perception from the contralateral legs was slightly higher, although it was not significant. In Table 2 higher values are shown: correlations of perception of temperature and pain from the contralateral foot is compared with all the other measured parameters.

In order to eliminate nonspecific correlations, observations in which all parameters were considered as absent were subtracted from the sample. For this subpopulation, 3 x 3 tables were constructed combining the altered and trace groups. The correlations of temperature and pain and vibratory perception dropped significant- ly, from 0.40 to 0.26, as well as correlation with touch perception from 0.47 to 0.18 (P < 0.01). On the contrary, the correlation between temperature and pain perception and tibial nerve SEP did not change (0.37 to 0.36). Also, the other correlations did not change significantly, i.e. vibratory perception and SEP, from 0,71 to 0.66, or touch perception and SEP, from 0.79 to 0.73. In addition it was noticeable that Pearson r coefficients were insignificantly lower when derived from 3 x 3 tables in comparison with 4 × 4 tables (Table 2).

At the beginning of the study, both peroneal and tibial nerve SEPs were recorded in every patient. After obtaining 100 observations from one half of the projected patient population, we compared the results of tibial and peroneal nerve SEPs with the per- ception of vibration from the foot and the tibia. The Pearson r value for correlation between tibial nerve SEPs and perception of vibration from the foot was 0.74, but for peroneal nerve SEP was significantly less, only 0.52 (P < 0.01). In addition, correlation between tibial SEPs and perception of vibration from the tibia was 0.67 while correla- tion between peroneal SEP and perception of vibration from tibia was again only 0.50, therefore we did not continue to record peroneal nerve SEPs.

338

TABLE 3

DISTRIBUTION OF TIBIAL SEP VERSUS VIBRATORY PERCEPTION AND TEMPERATURE AND PAIN PERCEPTION

NL a ALT + / - AB

Vibratory perception Sep Normal 9 4 0 0

Abnormal 9 16 12 8 Trace 0 5 4 11 Absent 0 3 15 123

Temperature and pain perception Sep Normal 3 3 0 7

Abnormal 4 15 1 25 Trace 0 7 2 11 Absent 1 12 2 119

a For abbreviations, see Table 1.

When the raw distributions from the 4 x 4 tables were analyzed for pairs of parameters, normal tibial nerve SEPs were not present with absent, or trace vibratory perception in a total of 219 observations (Table 3, top). Also, we did not observe any case when SEPs were trace or absent with normal vibratory perception. However, in the distribution of pain and temperature perception as one parameter, and tibial SEPs as the other, (Table 3, bottom) we found 7 patients who showed completely normal SEPs and completely absent temperature and pain perception, and one patient with normal temperature and pain perception and absent SEPs.

DISCUSSION

In this analysis of correlations between somatosensory perception and SEPs we chose SCI patients who were in a stationary stage of neural dysfunction. The common etiology and non-progressive nature of their disorder made the measurements more homogeneous than other studies of different diseases of the spinal cord (Dorfman et al. 1980; Fukushima and Mayanagi 1975; Halliday and Wakefield 1963; Mastaglia et al. 1978). On the other hand, the pattern of clinical dysfunction was variable and none of the patients showed distinct spinal dysfunctions (i.e. Brown-Sequard, anterior cord etc.), but usually the spinal cord dysfunction was severe and diffuse. About half of the population did not have any residual voluntary activity or sensory perception.

We tried to maintain strict criteria for normal values and to use age regression modified normative data. As we were interested in comparing the correlation of ipsi- lateral and contralateral temperature and pain perception with other parameters, we did not include patients with sacral and lumbar lesions, and our most caudal neurological level was T-12, to allow for the definite crossing of anterolateral tract fibers from the lower extremities below the level of the spinal lesion.

339

For sensory assessment we used quantitative techniques for measurement of vibratory thresholds, warm and cold thresholds, and heat and cold pain thresholds together with the known semi-quantitative technique of von Frey hair testing of light touch perception. These techniques showed acceptable repeatability in a normal popula- tion (Fagius and Warren 1981). We divided the observations into four different cate- gories. Similarly, some other studies (Rowed 1982; Young 1982) as well as our previous study (Dimitrijevi6 et al. 1983) used this approach. When we compared the results from 4 x 4 and 3 x 3 tables, the correlations were not significantly different, but 4 x 4 tables yielded higher values, justifying division into 4 categories instead of three.

If we compare our results with studies of acute spinal cord injuries there are certain differences. For example, the presence of SEP early in the course is a good prognostic sign for overall recovery, both in experimental (Bohlman etal. 1981; D'Angelo et al. 1973; Ducker et al. 1978; Kojima et al. 1979; Martin and Bloedel 1973) and clinical studies (Cadilhae et al. 1977; Perot and Vera 1982; Rowed 1982; Spielholz et al. 1979) although SEPs may be present even inthe absence of any sensory perception or antedate clinically detectable improvement in these patients (Rowed et al. 1978). On the contrary, in the chronic stage of dysfunction, SCI patients are adapted to their loss of spinal cord fibers and in our 110 patients we did not find a single case with normal SEP and absent or profound abnormality of vibratory sensibility or vice versa. Thus, if one of the tests is normal, the other would be redundant and we would not expect to find absent vibratory sensibility and normal SEP or absent SEP and normal vibratory sensibility. However, we found quite a few exceptions in the correlation of pain and temperature perception with other parameters, including several observations of absent pain and temperature perception together with normal SEPs. This confirms an expected poor correlation between evoked potentials and temperature and pairr perception (Halliday and Wakefield 1963; Halliday 1967; Larson et al. 1966). A comparison of sensory perception and evoked potentials in acute SCI with a follow-up to indicate a time period in which perception and SEPs would start to correlate, would probably tell us more about difference in underlying perceptual dysfunction in chronic versus acute SCI.

Good correlation between perception of touch, and vibration, and SEPs, and poorer correlation of temperature and pain perception with all the other parameters showed a clear segregation of modalities. This is a known fact from case studies (Halliday and Wakefield 1963; Larson et al. 1966; Mastaglia et al. 1978; Nathan et al. 1986; Pollock et al. 1953), but is difficult to demonstrate in a population study (Dimitrijevi6 et al. 1983). Further segregation between parameters was seen when we analyzed the subgroup of patients where all the patients with all responses absent were excluded. By this approach we tried to eliminate possible artefactually increased correlation due to positive correlation in patients where all responses were absent. There was not a significant change in correlations of vibratory perception and SEPs or touch perception and SEPs, thus justifying the initial inclusion criteria. On the contrary, the correlation between pain and temperature perception and vibratory sensibility or touch perception dropped significantly. However, the correlation between pain and tempera- ture perception and SEPs did not drop. It remained low but was still significant. This

340

corresponds well with some experimental and rare clinical studies showing a relation- ship between the pain and temperature perception (anterolateral system) and SEPs to electrical stimulation (Norrsell 1966; Schieppati and Ducati 1981). This low correlation did not allow us to use it clinically in case by case studies, but can explain some of the abnormal findings of possible different grouping of sensory modalities (Wall and Noordenbos 1977).

Another important finding is that abnormality of temperature and pain perception was present more often than abnormality of other modalities. This probably warrants further study of the correlation of temperature and pain perception with voluntary motor control (Vlahovitch et al. 1977) as well as residual motor functions responsible for spasticity in SCI patients.

The peroneal SEPs correlated significantly less with the somatosensory functions than the tibial SEPs. This supports the now more widely accepted use of tibial SEPs in SCI patients (Perot and Vera 1982; Rowed 1982) compared to the previous use of peroneal SEPs (Perot 1976). Another fact which might have contributed to the high correlations is that tibial nerve stimulation was biologically calibrated; its intensity was adjusted in such a way that it was possible to monitor the size of the motor response in one of the innervated muscles. Another reason might be that the tibial nerve was stimulated at the level of the knee where it is larger than at the ankle level, and by using a high intensity stimulation (maximal M response of the soleus muscle), we probably stimulated all available large fibers. In addition, at the popliteal fossa the tibial nerve is less prone to environmental temperature changes.

The study showed that in diffuse, severe SCI it was possible to obtain a high correlation between touch perception, vibratory perception, and SEPs which are all thought to share the dorsal columns as a common ascending pathway. A clear separation was shown for temperature and pain perception, which are known to be related to the spinothalamic system. However, the slightly different levels of correlation between all of these modalities, together with some residual correlation between temperature and pain perception and SEPs justify testing of at least these 4 different psychophysiological and neurophysiological modalities for assessment of residual sen- sory functions in SCI patients. This would be neccessary if any prognosis based on sensory functions for overall recovery is given in earlier stages of spinal cord injury.

ACKNOWLEDGEMENTS

The authors wish to thank the staff of the Department of Clinical Neuro- physiology T.I.R.R., Houston, TX, for excellent recordings and technical support. We are indebted to Mrs. Irena Herskowicz, MOTR for obtaining the sensory quantification data and to Mrs. Berit Lindblom for setting up the testing procedures. We thank Miss Debra Bernhard and Mrs. Helen Spencer for preparing the manuscript and Mr. Don Rossi for statistical analysis. We are grateful to Drs. Tine Prevec and Art Sherwood for helpful comments. The work was supported by the V.L. Smith Foundation for Restorative Neurology, Houston, TX.

341

REFERENCES

Bohlman, H.H., E. Bahniuk, G. Field and G. Raskulinecz (1981) Spinal cord monitoring of experimental incomplete cervical spinal cord injury. Spine, 6: 428-436.

Cadilhac, J., M. Georgesco, J. Benezech, M. Duday and G. Dapres (1977) Potential evoque cerebral somesthesique et reflexe d'Hoffmann dans les lesions medullaires aignes interet physiopathologique et pronostic. Electroencephalogr. Clin. NeurophysioL, 43: 160-167.

Cusick, J. F., J.B. Myklebust, S.J. Larson and A. Sauces (1979) Spinal cord evaluation by cortical evoked responses. Arch. Neurol., 36: 140-143.

D'Angelo, C.M., J. C. VanGilder and A. Tanb (1973) Evoked cortical potentials in experimental spinal cord trauma. J. Neurosurg., 38: 332-336.

Dimitrijevi6, M. R., T. S. Prevec and A.M. Sherwood (1983) Somatosensory perception and cortical evoked potentials in established paraplegia, J. Neurol. Sci., 60: 253-265.

Dorfman, L.J., I. Perkash, T.M. Bosley and K.L. Cummins (1980) Use of cerebral evoked potentials to evaluate spinal somatosensory function in patients with traumatic and surgical myelopathies. J. Neurosurg., 52: 654-660.

Ducker, T.B., M. Saleman, J.T. Lucas, W.B. Garrison and P.L. Perot (1978) Experimental spinal cord trauma. II: Blood flow, tissue oxygen, evoked potentials in both paretic and plegic monkeys. Surg. Neurol., 10: 64-70.

Fagius, J. and L.K. Warren (1981) Variability of sensory threshold determination in clinical use. J. Neurol. Sci., 51: 11-27.

Fruhstorfer, H., U. Lindblom and W.G. Schmidt (1976) Method for quantitative estimation of thermal thresholds in patients. J. Neurol. Neurosurg. Psych., 39: 1071-1075.

Fukushima, T. and Y. Mayanagi (1975) Neurophysiological examination (SEP) for the objective diagnosis of spinal lesions. In: Advances in Neurosurgery, (W. Klug, M. Brock, M. Klager and O. Spoerri Eds.), vol. 2, Springer-Verlag, Berlin, pp. 158-168.

Giblin, D.R. (1964) Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann. N. Y. Acad. Sci., 112: 93-141.

Goldberg, J.M. and U. Lindblom (1979) Standardised method of determining vibratory perception thresholds for diagnosis and screening in neurological investigation. J. Neurol. Neurosurg. Psych., 42: 793-803.

Halliday, A.M. (1967) Changes in the form of cerebral evoked responses in man associated with various lesions of the nervous system. In L. Widen (Ed.), Recent Advances in Clinical Neurophysiology, Electro- encephalogr. Clin. Neurophysiol., Suppl. 25: 178-192.

Halliday A.M. and G. S. Wakefield (1963) Cerebral evoked potentials in patients with dissociated sensory loss. J. NeuroL Neurosurg. Psych., 26:211-219.

Kojima, Y., T. Yamamoto, H. Ogino, K. Okada and K. Ono (1979) Evoked spinal potentials as a monitor of spinal cord viability. Spine, 4: 471-477.

Larson, S.J., A. Sauces and P.C. Christenson (1966) Evoked somatosensory potentials in man. Arch. Neurol., 15: 88-93.

Martin, S.H. and J.R. Bloedel (1973) Evaluation of experimental spinal cord injury using cortical evoked potentials. J. Neurosurg., 39: 75-81.

Mastaglia, F.L., J.L. Black, R. Edis and D.W.K. Collins (1978) The contribution of evoked potentials in the functional assessment of the somatosensory pathway. Clin. Exp. Neurol., 15: 279-298.

Nathan, P. W., M. C. Smith and A.W. Cook (1986) Sensory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain, 109: 1003-1041.

Norrsell, U. (1966) An evoked potential study of spinal pathways projected to the cerebral somatosensory areas in the dog. Exp. Brain Res., 2: 261-268.

Perot, P.L. (1976) Somatosensory evoked potentials in the evaluation of patients with spinal cord injury. In: Current Controversies in Neurosurgery, (T.P. Morley, ed.), W.B. Saunders, Philadalphia, pp.; 160-167.

Perot, P. L. and C. L. Vera (1982) Scalp-recorded somatosensory evoked potentials to stimulation of nerves in the lower extremities and evaluation of patients with spinal cord trauma. Ann. N. Y. Acad. Sci., 388: 359-368.

Pollock, L.J., B. Boshes, M. Brown, A.J. Arieff, I. Finkelman, H. Chor, N.B. Dobin, E.L. Tigay, B.H. Kesert, R.L. Crouch, H. Blustein, J.R. Finkle and S.W. Pyzik (1953) Evaluation of recovery of sensation to intraspinal pathways in injuries of the spinal cord. Arch. Neurol. Psych., 70: 137-150.

342

Rowed, D.W. (1982) Value of somatosensory evoked potentials for prognosis in partial cord injuries. In: Early Management of Acute Spinal Cord Injury, C. H. Tator, ed.), Raven Press, New York, pp. 167-180.

Rowed, D.W., J.A.G. McLean and C.H. Tator (1978) Somatosensory evoked potentials in acute spinal cord injury: Prognostic value. Surg. Neurol., 9: 203-210.

S chieppati, M. and A. Ducati (1981) Effects of stimulus intensity, cervical cord tractotomies and cerebellec- tomy on somatosensory evoked potentials from skin and muscle afferents of cat hind limb. Electroence- phalogr. Clin. Neurophysiol., 51: 363-372.

Shramm, J., K. Hashizume, T. Fukushima and H. Takahashi (1979) Experimental spinal cord injury produced by slow, graded compression. J. Neurosurg., 50: 48-57.

Spielholz, N.I., M.V. Benjamin, G. Engler and J. Ransohoff (1979) Somatosensory evoked potentials and clinical outcome in spinal cord injury. In: Neural Trauma, (A.J. Popp, Ed.), Raven Press, New York, pp. 217-222.

Stohr, M., V.W. Buettner, B. Riffel and E. Koletzki (1982) Spinal somatosensory evoked potentials in cervical cord lesions. Electroencephalogr. Clin. Neurophysiol., 54: 257-265.

Wall, P.D. and W. Noordenbos (1977) Sensory functions which remain in man after complete transection of dorsal columns. Brain, 100: 641-653.

Whitehorn, D., R.W. Morse and A.L. Towe (1969) Role of the spinocervical tract in production of the primary cortical response evoked by forepaw stimulation. Exp. NeuroL, 25: 349-364.

Vlahovitch, B., J.M. Fuentes, Y. Choucair and A.C. Verger (1977) Valeur pronostique indissociable des fonctions spinothalamique et corticospinale darts les traumatismes m6dullaires graves. Neurochirurgie, 23: 55-72.

Young, W. (1982) Correlation of somatosensory evoked potentials and neurological findings in spinal cord injury. In: Early Management of Acute Spinal Cord Injury, (C. H. Tator, ed.), Raven Press, New York, pp. 153-165.