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Somatosensory evoked responses to mechanical stimulation in normal subjects and in patients with neurological disorders
289
Journal of the neurological Sciences, 1974, 21 : 289 298 ,!~ Elsevier Scientific Publishing Company, Amsterdam
Printed in The Netherlands
Somatosensory Evoked Responses to Mechanical Stimulation in Normal Subjects and in Patients with Neurological Disorders TAKAO NAKANISHI, YASUO SHIMADA AND YASUO TOYOKURA Department qf Neurology, Institute of Brain Research School of Medicine, University of Tokyo Hongo, Tokyo, 113 (Japan) (Received 1 September, 1973)
INTRODUCTION
Most somatosensory evoked responses from the scalp in man have been elicited by electrical stimulation of mixed peripheral nerves. On the other hand, mechanical stimulation has been tried only by a few investigators (Alajouanine, Scherrer, Barbizet, Calvet and Verley 1958 ; Halliday and Mason 1964; Walter 1964; Desmedt, Debecker and Manil 1965 ; Ehrenberger, Finkenzeller, Keidel and Plattig 1966; Hrbek, Hrbkova and Lenard 1968; Meyjes 1969; Franzen and Offenloch 1969; Larsson and Prevec 1970; Matsumiya and Mostofsky 1972; Nakanishi, Takita and Toyokura 1973). In the previous paper (Nakanishi et al. 1973), somatosensory evoked responses to tactile taps applied to the middle finger were reported. The present study has been undertaken to investigate somatosensory evoked responses to pin-prick, touch and tactile tap applied to the middle finger and to the big toe in normal subjects and in patients with neurological disorders.
MATERIAL AND METHODS
The technique for tactile tap stimulation was the same as that used in the previous study (Nakanishi et al. 1973). For pin-prick and touch stimulation, an insect pin and a soft brush were fixed to the head of a AEL ONKYO vibrator, into which a 2 msec rectangular pulse from a pulse generator was fed. The tip of the pin and that of the soft brush were set in such a manner that the distance between these tips and the skin was about 1 mm before the pulse was passed into the vibrator. Motion of the head of the vibrator was perpendicular to the surface of the body with a displacement of 2.5 mm. Latency from the beginning of the motion to the peak was 3.5 msec. These mechanical stimuli were delivered every 1.5 sec to the dorsum of the middle phalanx of the middle finger and to the dorsum of the proximal phalanx of the big toe with a contact This work was supported by a grant for scientific research from the Ministry of Education of Japan.
290
T. NAKANISHI, Y. SHIMADA, Y. TOYOKURA
time of a few msec. The vibrator was mounted in a steel box, and the stimulation was almost inaudible. The contralateral evoked potentials were recorded bipolarly with electrodes located at FC3-C3 o r F C 4 - - C 4 according to the internationally accepted 10-20 electrode system for middle finger stimulation and with those located at FC~ ( for big toe stimulation. This is based on the reason that a phase reversal for the response to the finger or to the toe stimulation was observed at Cn in relation ~,~ thc 1~-20 electrode system of electrode placement and the response was easily recorded bipolarly with an electrode combination of FC, Co with good reproducibility in mosl subjects. The electrode connection to the amplifiers was arranged so that an upward deflection meant positivity of the C, relative to the FC, electrode. The recording system was the same as that used in the previous study (Nakanishi et al. 1973). Each record was the sum of 200 consecutive responses, each recorded over a period of 80 msec following the stimulus. Control recordings of possible auditory evoked response contamination were made without visible response. For comparing mechanically evoked potentials with those evoked by electrical stimulation, the electrical stimulation was applied to the median nerve with the same method as that used in the previous study (Nakanishi et al. 1973), and it was also applied to the sural nerve at the external retromalleolar groove with the same intensity as that used to stimulate the median nerve. The individuals examined were 33 normal young volunteers, 9 male and 24 female, ranging in age from 19 to 32 with a median of 23 years, and 61 patients with neurological disorders. These included 11 cases with peripheral neuropathy, 23 cases with lesions of the spinal cord or the brain stem and 27 cases with cerebral lesions.
RESULTS
In normal subjects Fig. 1 shows contralateral typical evoked responses to mechanical stimuli applied to the middle finger and to the big toe, and those to electrical stimulation delivered to the median nerve and to the sural nerve in a normal subject. The responses evoked by mechanical stimuli were very similar to those evoked by peripheral nerve stimulation. It started with a small surface negative deflection (not always present) followed by a large surface positive wave, which was formed as a reversed W shape in most subjects. The well-defined responses to middle finger stimulation were evoked by pin-prick and by tactile tap in all subjects examined, but by touch in only 69 ~o; those to big toe stimulation were evoked by pin-prick in 93/o, o/ by tactile tap in 88 ~,~ and by touch in 77 ~ . Generally, the incidence of appearance of the evoked responses to mechanical stimuli was slightly lower than that to electrical stimulation which was ibund with 1 0 0 ~ of stimuli. In this study, the positive wave with the reversed W-shaped response was analysed. The peaks of the deflection in this response were labelled N 1 for the initial surface negative deflection, P1 for the first positive, N2 for the second negative and Pz for the second positive respectively. The peak latency of P1 to the middle finger stimulation was: 32.2 ___3.7 msec for tactile tap, 35.5 ___4.0 msec for pin-prick and 35.9 ± 4.5 msec for touch; and that to the big toe stimulation was: 4 9 . 6 _ 4.6 msec for tactile tap, 50.3
291
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
Middle Finger
Tactile
Big
TOe
Tap
Pin-Prick
Touch
Elect, SI, ~
T
2,5 ~a~V
Fig. 1. Contralateral typical responses to mechanical stimuli applied to the middle finger and the big toe, and those to electrical stimulation delivered to the median and the sural nerves in a normal subject. An upward deflection means positivity of the C. relative to the FC, electrode. Note latency differences of comparable peaks between these recordings.
TABLE 1 PEAK LATENCIES
(in msec) oF VARIOUS COMPENENTS OF
THE REVERSED W - S H A P E D RESPONSE EVOKED BY M E C H A -
N I C A L A N D ELECTRICAl, STIMULATION
Right side stimulated. The latencies of the response to pin-prick and to touch have"not been corrected for the analysis delay (0.5-2 msec).
Middle finger tactile tap pin-prick touch N. medianus electr, stimulation
Big toe tactile tap pin-prick touch N. suralis electr, stimulation
P2
No. of Subjects
39.1 _+4.2 43.5_+5.1 45.4_+4.1
48.7-+3.3 55.7-+4.1 56.2_+4.4
21 24 14
24.6_+2.5
33.9_+3.8
43.8_+5.2
17
41.3_+5.2 43.4_+7.3 54.1-+8.3
49.6_+4.6 50.3_+7.5 60.3+8.1
60.4_+6.2 59.9_+9.3 71.6+9.0
74.1 4- 10.1 69.8-+10.9 80.0-+ 8.1
t4 8 6
33.1+2.6
41.6+3.9
52.5+5.7
64.5-+ 5.2
16
N~
P1
24.4_+2.3 27.4-+2.5 29.1 _+3.3
32.2-+3.7 35.5-+4.0 35.9_+4.5
18.1 _+0.8
Nz
292
T. NAKANISHI, Y. SHIMADA, Y. TOYOKURA
__+7.5 msec for pin-prick and 60.3 ± 8.1 msec for touch respectively (Table 1). The latencies of the responses to the mechanical stimuli were longer than those for the electrical stimulus. The peak-to-peak amplitudes measured from the peak of the initial surface negativity to the peak of the following positivity (N,-P,) for middle finger stimulation were : 1.8+0.9/~V for tactile tap, 1.4_+0.7 #V pin-prick and 0.7_+0.4 #V for touch; and those for big toe stimulation were: 0.6_+0.3 #xV for tactile tap, 0.7__+0.3 IN for pinprick and 0.5 _+0.2 yV for touch (Table 2). The responses to the mechanical stimuli were of smaller amplitude than those for the electrical stimulus. TABLE 2
(in laV) OF THE REVERSED
AVERAGES OF THE PEAK-TO-PEAK AMPLITUDE
W-SHAPED RESPONSE ~OR TWO KINDS
Or STIMULATION Right side stimulated, Pi'-N2
NI-Pl .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
7
.
.
.
.
No. ~tt
N2 P2 .
.
.
.
.
.
.
subiect,~ .
.
.
.
.
.
.
.
.
.
.
Middle finger
tactile tap pin-prick touch
1.8+_0.9 1.4+_0.7 0.7+-0.4
0.7_+0.5 0.9___0.6 0.7+_0.4
1.4+_0.6 1.6__+0.7 1.0_+0.5
2t 24 14
6.6+-2.6
3.9+-2.3
3.7+_2.(I
I7
I).6_+0.3 0.7_+0.3 0.5_+0.2
1.2+_0,6 1.2_+0.7 0.9+_0.5
0.8_+0.6 0.9+_0.4 0.8_+0.5
14 x 0
N. medianus
electr, stimulation
Bi9 toe
tactile tap pin-prick touch A,. surali,~.
.
.
electr, stimulation
.
.
.
.
1.3_+0.7
.
.
.
2.0_+ 1.1
.
.
.
t . 7 _ 1.4
.
.
16
The peak latencies and the wave forms of the reversed W-shaped potential evoked by mechanical stimuli to both sides of the middle finger and of the big toe were almost bilaterally symmetrical. The amplitudes, however, were different between both sides of the hemispheres in each subject, but almost equal statistically. The ratio of the amplitude of the response in the left hemisphere to the mean of those recorded over both hemispheres was 1.04-t-0.24.
In patients with neurological disorders In 11 patients with peripheral neuropathy, of whom 7 patients had intact joint position sense, the somatosensory evoked responses to mechanical stimuli were altered in one or more of three following ways: delayed latency, reduced amplitude, or abnormal wave form; especially in delayed latency. Fig. 2 shows a marked increased latency of the responses in a patient with interstitial hypertrophic neuritis. It differs in latency by about 25 msec for middle finger stimulation, compared with a standard deviation of 2 to 5 msec in the normal subjects. When there was severe sensory loss, the respon-
293
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
Touch
Elect, S t i
ili
200 ~ e ~
ii
....
Fig. 2. Evoked responses in a patient with interstitial hypertrophic neuritis. Note abnormally prolonged latencies of the responses with almost normal wave form and amplitude.
ses were completely abolished. The results obtained by mechanical stimuli correlated well with the modality and the severity of the sensory deficit detected by clinical examination. Twenty-three patients with lesions of the spinal cord or the brain stem were divided into 2 groups according to the type of sensory deficit found on clinical examination. One consisted of 15 patients with impairment of all modalities of sensation including joint position sense, and the other, 8 patients with preserved joint position sense but impaired pain-temperature and touch sensation. In 15 patients with impaired joint position sense, the somatosensory evoked responses to mechanical and electrical stimulation were affected in ways similar to those observed in patients with peripheral neuropathy. However, there was I patient among them, in whom the evoked response to pin-prick was different from that to electrical stimulation as shown in Fig. 3. She had loss of joint position sense and touch sensation to pin-prick stimulation in the right leg; in her case the cortical potentials were not evoked by electrical stimulation but were produced by pin-prick stimulation. On the other hand, in 7 of the 8 patients with preserved joint position sense, the evoked responses to mechanical stimuli were also altered in similar ways. Fig. 4 shows the loss of the normal somatosensory evoked responses on the affected side of the shoulder area in a patient with syringomyelia, in whom pain-temperature and touch sensation were impaired and joint position sense was preserved. In 2 of the 3 patients with syringomyelia who had a similar dissociated sensory deficit, similar findings were obtained. In a patient with an intramedullary tumour of the spinal cord who had impaired pain-temperature and touch sensation
294
T. NAKANISHt. Y. SHIMADA, Y. I'OYOKURA A | t ~ ¢ l e d SiOe
Normal carrie
Fig. 3. Evoked responses in a patient with an intramedullary tumour of the spinal cord, who had loss of joint position sense and touch feeling to pin-prick stimulation in the right leg. Cortical evoked potentials were not obtained by electrical stimulation, but by pin-prick stimulation on the affected side
Fig. 4. Evoked responses showing the loss of the normal somatosensory evoked responses on stim ulation of the affected shoulder area in a patient with syringomyelia, in whom pain-temperature and touch sensation were impaired and joint position sense was preserved. The contralateral evoked potentials were recorded bipolarly with electrodes located at FC~ C~ or FC2-C2.
and intact joint position sense, the cortical potentials were evoked by electrical stimulation but not by mechanical stimulation of the affected leg (Fig. 5). On the other hand, in a patient with the Wallenberg syndrome, who had loss of pain-temperature sensation with intact touch and joint position sense on the right side, the somatosensory evoked responses to mechanical stimulation, including pin-prick stimulation, were
295
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
A f f e c t e d Side
Normal S i d e
Ta~t ile Tap
Pin- Prick
Touch
Elect St. N. Suralis
z.s ,uv l
!
100 rn sec
Fig. 5. Evoked responses in a patient with an intramedullary tumour of the spinal cord, who had intact position sense and impaired pain-temperature and touch sensation in the left leg. Cortical potentials were evoked by electrical stimulation, but not by mechanical stimulation on the affected side.
apparently unaffected on the side corresponding to the loss of pain-temperature sensation. Twenty-seven patients with cerebral lesions examined were divided into 2 groups according to the clinical sensory examination. One group consisted of 9 patients without sensory impairment. These included 5 patients with vascular malformations, 3 with brain tumour and one with porencephaly. The somatosensory evoked responses obtained in this group were apparently unaffected. The other group consisted of 18 patients with unilateral sensory impairment. There were 10 patients with vascular lesions and 8 with brain tumours. The somatosensory evoked responses obtained on the affected side in this series of patients were divided into 3 types according to the grade of their abnormality. The first type of response was normal or near normal, and was seen in 3 patients. The second type of response was a relatively abnormal wave form of the response to stimulation of the affected side. This type of response was seen in 10 patients. The third type of response was a complete absence or a profound alteration of all components to stimulation of the affected side. Fig. 6 shows the abolished or much reduced potentials in a patient who had a lesion of the thalamus due to a vascular malformation. The somatosensory evoked responses to mechanical stimulation in this series of patients correlated well with the severity of the sensory impairment.
DISCUSSION
In normal subjects Cortical potentials evoked by mechanical stimuli, such as pin-prick, touch and tactile tap could be detected by the method used in this study. The fact that these
296
T. NAKANISHI, Y. SHIMADA, Y. TOYOKURA
Fig. 6. Evoked responses in a patient with lesion of the thalamus due to a vascular malformation Abolished or very much reduced potentials were obtained by stimulation of the affected side.
responses cannot be obtained always in normal subjects, however, must be kept in mind in assessing the clinical application of the method. The initial peak latency (N 1) of the reversed W-shaped response to pin-prick stimulation applied to the middle finger was 27.4 ± 2.5 msec, being very similar to th at evoked with the pin used by Meyjes (1969). The latency value of 32.2 ± 3.7 msec for P~ obtained by tactile tap stimulation to the middle finger was a little shorter than that given by pin-prick and touch stimulation. It might have been due to the uncorrected analysis delo,y from the vibrator. The peak latency for P ~ of the response to pin-prick applied to the finger was 36 msec and that applied to the big toe 50 msec. This gives a conductton time difference of 14 msec, which is reasonable if one considers that the distance between two sites is about 70 cm.
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
297
In our previous paper (Nakanishi et al. 1973), we mentioned that the amplitude of the contralateral evoked response was greater over the left hemisphere in most subjects. In this study with a larger number of subjects examined, however, the amplitudes of the response to the three types of mechanical stimulation were almost equal statistically over both hemispheres, although they were greatly changed in each subject. In patients with neurological disorders The results obtained in this study with regard to a correlation between sensory deficit and alterations in the somatosensory evoked responses to mechanical stimulation in patients with peripheral neuropathy and with cerebral lesions are in general agreement with previous investigations of the responses evoked by electrical stimulation (Giblin 1964; Williamson, Goff and Allison 1970). The findings in patients with dissociated sensory loss due to lesions of the spinal cord, however, were somewhat different from those obtained by electrical stimulation (Halliday and Wakefield 1963 ; Giblin 1964; Larson, Sances and Christenson 1966). Alteration of the somatosensory evoked responses to mechanical stimulation was observed in 7 of the 8 patients with impaired pain-temperature and touch sensation but preserved joint position sense. In a patient with such a dissociated sensory deficit, the cortical potentials were evoked by electrical stimulation, but not by mechanical stimulation on the affected side (Fig. 5). On the other hand, in a patient with loss of joint position se,qse and impaired touch and pain-temperature sensation, the cortical potentials were elicited by pin-prick stimulation, but not by electrical stimulation (Fig. 3). These findings might suggest that the afferent impulses responsible for the somatosensory evoked responses to mechanical stimulation travel by the ventro-lateral tracts. One patient with the Wallenberg syndrome, in whom pain-temperature sensation was lost and touch and joint position sense were intact, had normal somatosensory evoked responses. However, it might be due to the fact that pin-prick stimulation excites many and various types of receptors for touch and tap sensation as well as those for pain. In other words, normal somatosensory evoked responses to pin-prick stimulation in this case might depend upon the integrity of the pathways mediating touch and tap sensation. The good correlation between clinical sensory deficit and alterations in the somatosensory evoked responses to mechanical stimulation obtained in this study might provide a basis for future clinical use of this technique.
SUMMARY
The contralateral somatosensory evoked responses to mechanical stimuli, such as pin-prick, touch and tactile tap, applied to the middle finger and to the big toe were studied in 33 normal young volunteers and in 61 patients with neurological disorders, with emphasis on the early components of the response. In normal subjects, the well-defined cortical responses to mechanical stimuli could be obtained by the method used in this study, but the consistency with which the responses could be recorded was a little lower than in the case of electrical stimulation. In each subject, the bilateral peak latencies and wave forms were almost equal,
298
T. NAKANISHI, Y. SHIMADA, Y. I-t)YOKURA
whereas the amplitudes were greatly changed over the two hemispheres The results obtained in this study with regard to a correlation between sensory defi-~ cit and alterations in the somatosensory evoked responses to mechanical stimulation in patients with peripheral neuropathy and with cerebral lesions are in general agreement with previous investigations of the responses evoked by electrical stimulation The findings in patients with dissociated sensory loss due to the spinal cord lesions suggest that the afferent impulses responsible for the somatosensory evoked responses to mechanical stimulation travel by the ventro-lateral tracts.
REFERENCES ALAJOUANINE,T., J. SCHERRER,J. BARBIZEI, J. CALVETAND R. VERLEY(1958) Potentiels evoqu6s corticaux chez des subjets atteints de troubles somesth6siques, Rev. neurol., 98: 757-761. DESMEDT, J. E., J. DEBECKERAND J. MANIt. (1965) Mise en 6vidence d'un signe 61ectrique cer6bral associ6 il la d+tection par le sujet, d'un stimulus sensoriel tactile, Bull. Acad. reed. belg., 5: 887-936. EHRENBERGER, K., P. FINKENZELLER, W. D. KEIDEL AND K. H. PI.ATTIG (1966) Elektrophysiologische Korrelation der Stevensschen Potenzfunktion und objektive Schwellenmessung am Vibrationssinn des Menschen, Pfliigers Arch. ges. PhysioL, 290: 114-123. FRANZ~N, O. AND K. OF~NLOCrt (1969) Evoked response correlates of psychophysical magnitude estimates for tactile stimulation in man, Exp. Brain Res, 8: 1--18. GmLIN, 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. HALLIDAY, A. M. AND A. A. MASON (1964) The effect of hypnotic anaesthesia on cortical responses, .L Neurol. Neurosurg. Psychiat., 27:300 312. HALLtDAV, A. M. AND G. S. WAKEHELD(1963) Cerebral evoked potentials in patients with dissociated sensory loss, J. Neurol. Neurosurg. Psychiat., 26:211 219. HRBEK, A., M. HRBKOVAAND H. G. LENARD (1968) Somatosensory evoked responses in newborn infants. Electroenceph. clin. Neurophysiol., 25: 443-448. LARSON. JR., S., J. SANCFS AND P. C. CttRtSFENSON (1966) Evoked somatosensory potentials m man Arch. NeuroL (Chic.), 15:88 93. LARSSON, L. E. AND T. S. PREVEC (1970) SoMArO-sensory response to mechanical stimulation as recorded in human EEG, Electroenceph. clin. NeurophysioL, 28: 162-172, MATSUMIYA,Y. AND D. I. MOSTOFSKY(1972) Somatosensory evoked responses elicited by corneal and nostril air puff stimulation, Electroenceph. clin. NeurophysioL, 33 : 225-227. MEYJES, JR., F. E. P. (1969) Some characteristics of the early components of the somato-sensory evoked response to mechanical stimuli in man. Psychiat. Neurol. Neurochir. (Amst), 72:263 268~ NAKANISHLT., K. TAKITAAND Y. TOYOKURA(1973) Somatosensory evoked responses to tactile tap in man, Electroenceph. clin. Neurophysiol., 3 4 : 1 6. WALTER,W. G. (1964) The convergence and interaction of visual, auditory, and tactile responses in human nonspecific cortex, Ann. N.Y. Acad. Sci., I 12: 320- 361. WILLIAMSON,P. D., W. R. GOFF ANt) T, ALLISON (1970) Somatosensory evoked responses in patients with unilateral cerebral lesions, Electroenceph. olin. NcurophysioL. 28 : 566 575.
Journal of the neurological Sciences, 1974, 21 : 289 298 ,!~ Elsevier Scientific Publishing Company, Amsterdam
Printed in The Netherlands
Somatosensory Evoked Responses to Mechanical Stimulation in Normal Subjects and in Patients with Neurological Disorders TAKAO NAKANISHI, YASUO SHIMADA AND YASUO TOYOKURA Department qf Neurology, Institute of Brain Research School of Medicine, University of Tokyo Hongo, Tokyo, 113 (Japan) (Received 1 September, 1973)
INTRODUCTION
Most somatosensory evoked responses from the scalp in man have been elicited by electrical stimulation of mixed peripheral nerves. On the other hand, mechanical stimulation has been tried only by a few investigators (Alajouanine, Scherrer, Barbizet, Calvet and Verley 1958 ; Halliday and Mason 1964; Walter 1964; Desmedt, Debecker and Manil 1965 ; Ehrenberger, Finkenzeller, Keidel and Plattig 1966; Hrbek, Hrbkova and Lenard 1968; Meyjes 1969; Franzen and Offenloch 1969; Larsson and Prevec 1970; Matsumiya and Mostofsky 1972; Nakanishi, Takita and Toyokura 1973). In the previous paper (Nakanishi et al. 1973), somatosensory evoked responses to tactile taps applied to the middle finger were reported. The present study has been undertaken to investigate somatosensory evoked responses to pin-prick, touch and tactile tap applied to the middle finger and to the big toe in normal subjects and in patients with neurological disorders.
MATERIAL AND METHODS
The technique for tactile tap stimulation was the same as that used in the previous study (Nakanishi et al. 1973). For pin-prick and touch stimulation, an insect pin and a soft brush were fixed to the head of a AEL ONKYO vibrator, into which a 2 msec rectangular pulse from a pulse generator was fed. The tip of the pin and that of the soft brush were set in such a manner that the distance between these tips and the skin was about 1 mm before the pulse was passed into the vibrator. Motion of the head of the vibrator was perpendicular to the surface of the body with a displacement of 2.5 mm. Latency from the beginning of the motion to the peak was 3.5 msec. These mechanical stimuli were delivered every 1.5 sec to the dorsum of the middle phalanx of the middle finger and to the dorsum of the proximal phalanx of the big toe with a contact This work was supported by a grant for scientific research from the Ministry of Education of Japan.
290
T. NAKANISHI, Y. SHIMADA, Y. TOYOKURA
time of a few msec. The vibrator was mounted in a steel box, and the stimulation was almost inaudible. The contralateral evoked potentials were recorded bipolarly with electrodes located at FC3-C3 o r F C 4 - - C 4 according to the internationally accepted 10-20 electrode system for middle finger stimulation and with those located at FC~ ( for big toe stimulation. This is based on the reason that a phase reversal for the response to the finger or to the toe stimulation was observed at Cn in relation ~,~ thc 1~-20 electrode system of electrode placement and the response was easily recorded bipolarly with an electrode combination of FC, Co with good reproducibility in mosl subjects. The electrode connection to the amplifiers was arranged so that an upward deflection meant positivity of the C, relative to the FC, electrode. The recording system was the same as that used in the previous study (Nakanishi et al. 1973). Each record was the sum of 200 consecutive responses, each recorded over a period of 80 msec following the stimulus. Control recordings of possible auditory evoked response contamination were made without visible response. For comparing mechanically evoked potentials with those evoked by electrical stimulation, the electrical stimulation was applied to the median nerve with the same method as that used in the previous study (Nakanishi et al. 1973), and it was also applied to the sural nerve at the external retromalleolar groove with the same intensity as that used to stimulate the median nerve. The individuals examined were 33 normal young volunteers, 9 male and 24 female, ranging in age from 19 to 32 with a median of 23 years, and 61 patients with neurological disorders. These included 11 cases with peripheral neuropathy, 23 cases with lesions of the spinal cord or the brain stem and 27 cases with cerebral lesions.
RESULTS
In normal subjects Fig. 1 shows contralateral typical evoked responses to mechanical stimuli applied to the middle finger and to the big toe, and those to electrical stimulation delivered to the median nerve and to the sural nerve in a normal subject. The responses evoked by mechanical stimuli were very similar to those evoked by peripheral nerve stimulation. It started with a small surface negative deflection (not always present) followed by a large surface positive wave, which was formed as a reversed W shape in most subjects. The well-defined responses to middle finger stimulation were evoked by pin-prick and by tactile tap in all subjects examined, but by touch in only 69 ~o; those to big toe stimulation were evoked by pin-prick in 93/o, o/ by tactile tap in 88 ~,~ and by touch in 77 ~ . Generally, the incidence of appearance of the evoked responses to mechanical stimuli was slightly lower than that to electrical stimulation which was ibund with 1 0 0 ~ of stimuli. In this study, the positive wave with the reversed W-shaped response was analysed. The peaks of the deflection in this response were labelled N 1 for the initial surface negative deflection, P1 for the first positive, N2 for the second negative and Pz for the second positive respectively. The peak latency of P1 to the middle finger stimulation was: 32.2 ___3.7 msec for tactile tap, 35.5 ___4.0 msec for pin-prick and 35.9 ± 4.5 msec for touch; and that to the big toe stimulation was: 4 9 . 6 _ 4.6 msec for tactile tap, 50.3
291
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
Middle Finger
Tactile
Big
TOe
Tap
Pin-Prick
Touch
Elect, SI, ~
T
2,5 ~a~V
Fig. 1. Contralateral typical responses to mechanical stimuli applied to the middle finger and the big toe, and those to electrical stimulation delivered to the median and the sural nerves in a normal subject. An upward deflection means positivity of the C. relative to the FC, electrode. Note latency differences of comparable peaks between these recordings.
TABLE 1 PEAK LATENCIES
(in msec) oF VARIOUS COMPENENTS OF
THE REVERSED W - S H A P E D RESPONSE EVOKED BY M E C H A -
N I C A L A N D ELECTRICAl, STIMULATION
Right side stimulated. The latencies of the response to pin-prick and to touch have"not been corrected for the analysis delay (0.5-2 msec).
Middle finger tactile tap pin-prick touch N. medianus electr, stimulation
Big toe tactile tap pin-prick touch N. suralis electr, stimulation
P2
No. of Subjects
39.1 _+4.2 43.5_+5.1 45.4_+4.1
48.7-+3.3 55.7-+4.1 56.2_+4.4
21 24 14
24.6_+2.5
33.9_+3.8
43.8_+5.2
17
41.3_+5.2 43.4_+7.3 54.1-+8.3
49.6_+4.6 50.3_+7.5 60.3+8.1
60.4_+6.2 59.9_+9.3 71.6+9.0
74.1 4- 10.1 69.8-+10.9 80.0-+ 8.1
t4 8 6
33.1+2.6
41.6+3.9
52.5+5.7
64.5-+ 5.2
16
N~
P1
24.4_+2.3 27.4-+2.5 29.1 _+3.3
32.2-+3.7 35.5-+4.0 35.9_+4.5
18.1 _+0.8
Nz
292
T. NAKANISHI, Y. SHIMADA, Y. TOYOKURA
__+7.5 msec for pin-prick and 60.3 ± 8.1 msec for touch respectively (Table 1). The latencies of the responses to the mechanical stimuli were longer than those for the electrical stimulus. The peak-to-peak amplitudes measured from the peak of the initial surface negativity to the peak of the following positivity (N,-P,) for middle finger stimulation were : 1.8+0.9/~V for tactile tap, 1.4_+0.7 #V pin-prick and 0.7_+0.4 #V for touch; and those for big toe stimulation were: 0.6_+0.3 #xV for tactile tap, 0.7__+0.3 IN for pinprick and 0.5 _+0.2 yV for touch (Table 2). The responses to the mechanical stimuli were of smaller amplitude than those for the electrical stimulus. TABLE 2
(in laV) OF THE REVERSED
AVERAGES OF THE PEAK-TO-PEAK AMPLITUDE
W-SHAPED RESPONSE ~OR TWO KINDS
Or STIMULATION Right side stimulated, Pi'-N2
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The peak latencies and the wave forms of the reversed W-shaped potential evoked by mechanical stimuli to both sides of the middle finger and of the big toe were almost bilaterally symmetrical. The amplitudes, however, were different between both sides of the hemispheres in each subject, but almost equal statistically. The ratio of the amplitude of the response in the left hemisphere to the mean of those recorded over both hemispheres was 1.04-t-0.24.
In patients with neurological disorders In 11 patients with peripheral neuropathy, of whom 7 patients had intact joint position sense, the somatosensory evoked responses to mechanical stimuli were altered in one or more of three following ways: delayed latency, reduced amplitude, or abnormal wave form; especially in delayed latency. Fig. 2 shows a marked increased latency of the responses in a patient with interstitial hypertrophic neuritis. It differs in latency by about 25 msec for middle finger stimulation, compared with a standard deviation of 2 to 5 msec in the normal subjects. When there was severe sensory loss, the respon-
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SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
Touch
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Fig. 2. Evoked responses in a patient with interstitial hypertrophic neuritis. Note abnormally prolonged latencies of the responses with almost normal wave form and amplitude.
ses were completely abolished. The results obtained by mechanical stimuli correlated well with the modality and the severity of the sensory deficit detected by clinical examination. Twenty-three patients with lesions of the spinal cord or the brain stem were divided into 2 groups according to the type of sensory deficit found on clinical examination. One consisted of 15 patients with impairment of all modalities of sensation including joint position sense, and the other, 8 patients with preserved joint position sense but impaired pain-temperature and touch sensation. In 15 patients with impaired joint position sense, the somatosensory evoked responses to mechanical and electrical stimulation were affected in ways similar to those observed in patients with peripheral neuropathy. However, there was I patient among them, in whom the evoked response to pin-prick was different from that to electrical stimulation as shown in Fig. 3. She had loss of joint position sense and touch sensation to pin-prick stimulation in the right leg; in her case the cortical potentials were not evoked by electrical stimulation but were produced by pin-prick stimulation. On the other hand, in 7 of the 8 patients with preserved joint position sense, the evoked responses to mechanical stimuli were also altered in similar ways. Fig. 4 shows the loss of the normal somatosensory evoked responses on the affected side of the shoulder area in a patient with syringomyelia, in whom pain-temperature and touch sensation were impaired and joint position sense was preserved. In 2 of the 3 patients with syringomyelia who had a similar dissociated sensory deficit, similar findings were obtained. In a patient with an intramedullary tumour of the spinal cord who had impaired pain-temperature and touch sensation
294
T. NAKANISHt. Y. SHIMADA, Y. I'OYOKURA A | t ~ ¢ l e d SiOe
Normal carrie
Fig. 3. Evoked responses in a patient with an intramedullary tumour of the spinal cord, who had loss of joint position sense and touch feeling to pin-prick stimulation in the right leg. Cortical evoked potentials were not obtained by electrical stimulation, but by pin-prick stimulation on the affected side
Fig. 4. Evoked responses showing the loss of the normal somatosensory evoked responses on stim ulation of the affected shoulder area in a patient with syringomyelia, in whom pain-temperature and touch sensation were impaired and joint position sense was preserved. The contralateral evoked potentials were recorded bipolarly with electrodes located at FC~ C~ or FC2-C2.
and intact joint position sense, the cortical potentials were evoked by electrical stimulation but not by mechanical stimulation of the affected leg (Fig. 5). On the other hand, in a patient with the Wallenberg syndrome, who had loss of pain-temperature sensation with intact touch and joint position sense on the right side, the somatosensory evoked responses to mechanical stimulation, including pin-prick stimulation, were
295
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
A f f e c t e d Side
Normal S i d e
Ta~t ile Tap
Pin- Prick
Touch
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Fig. 5. Evoked responses in a patient with an intramedullary tumour of the spinal cord, who had intact position sense and impaired pain-temperature and touch sensation in the left leg. Cortical potentials were evoked by electrical stimulation, but not by mechanical stimulation on the affected side.
apparently unaffected on the side corresponding to the loss of pain-temperature sensation. Twenty-seven patients with cerebral lesions examined were divided into 2 groups according to the clinical sensory examination. One group consisted of 9 patients without sensory impairment. These included 5 patients with vascular malformations, 3 with brain tumour and one with porencephaly. The somatosensory evoked responses obtained in this group were apparently unaffected. The other group consisted of 18 patients with unilateral sensory impairment. There were 10 patients with vascular lesions and 8 with brain tumours. The somatosensory evoked responses obtained on the affected side in this series of patients were divided into 3 types according to the grade of their abnormality. The first type of response was normal or near normal, and was seen in 3 patients. The second type of response was a relatively abnormal wave form of the response to stimulation of the affected side. This type of response was seen in 10 patients. The third type of response was a complete absence or a profound alteration of all components to stimulation of the affected side. Fig. 6 shows the abolished or much reduced potentials in a patient who had a lesion of the thalamus due to a vascular malformation. The somatosensory evoked responses to mechanical stimulation in this series of patients correlated well with the severity of the sensory impairment.
DISCUSSION
In normal subjects Cortical potentials evoked by mechanical stimuli, such as pin-prick, touch and tactile tap could be detected by the method used in this study. The fact that these
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Fig. 6. Evoked responses in a patient with lesion of the thalamus due to a vascular malformation Abolished or very much reduced potentials were obtained by stimulation of the affected side.
responses cannot be obtained always in normal subjects, however, must be kept in mind in assessing the clinical application of the method. The initial peak latency (N 1) of the reversed W-shaped response to pin-prick stimulation applied to the middle finger was 27.4 ± 2.5 msec, being very similar to th at evoked with the pin used by Meyjes (1969). The latency value of 32.2 ± 3.7 msec for P~ obtained by tactile tap stimulation to the middle finger was a little shorter than that given by pin-prick and touch stimulation. It might have been due to the uncorrected analysis delo,y from the vibrator. The peak latency for P ~ of the response to pin-prick applied to the finger was 36 msec and that applied to the big toe 50 msec. This gives a conductton time difference of 14 msec, which is reasonable if one considers that the distance between two sites is about 70 cm.
SOMATOSENSORY EVOKED RESPONSES TO MECHANICAL STIMULATION
297
In our previous paper (Nakanishi et al. 1973), we mentioned that the amplitude of the contralateral evoked response was greater over the left hemisphere in most subjects. In this study with a larger number of subjects examined, however, the amplitudes of the response to the three types of mechanical stimulation were almost equal statistically over both hemispheres, although they were greatly changed in each subject. In patients with neurological disorders The results obtained in this study with regard to a correlation between sensory deficit and alterations in the somatosensory evoked responses to mechanical stimulation in patients with peripheral neuropathy and with cerebral lesions are in general agreement with previous investigations of the responses evoked by electrical stimulation (Giblin 1964; Williamson, Goff and Allison 1970). The findings in patients with dissociated sensory loss due to lesions of the spinal cord, however, were somewhat different from those obtained by electrical stimulation (Halliday and Wakefield 1963 ; Giblin 1964; Larson, Sances and Christenson 1966). Alteration of the somatosensory evoked responses to mechanical stimulation was observed in 7 of the 8 patients with impaired pain-temperature and touch sensation but preserved joint position sense. In a patient with such a dissociated sensory deficit, the cortical potentials were evoked by electrical stimulation, but not by mechanical stimulation on the affected side (Fig. 5). On the other hand, in a patient with loss of joint position se,qse and impaired touch and pain-temperature sensation, the cortical potentials were elicited by pin-prick stimulation, but not by electrical stimulation (Fig. 3). These findings might suggest that the afferent impulses responsible for the somatosensory evoked responses to mechanical stimulation travel by the ventro-lateral tracts. One patient with the Wallenberg syndrome, in whom pain-temperature sensation was lost and touch and joint position sense were intact, had normal somatosensory evoked responses. However, it might be due to the fact that pin-prick stimulation excites many and various types of receptors for touch and tap sensation as well as those for pain. In other words, normal somatosensory evoked responses to pin-prick stimulation in this case might depend upon the integrity of the pathways mediating touch and tap sensation. The good correlation between clinical sensory deficit and alterations in the somatosensory evoked responses to mechanical stimulation obtained in this study might provide a basis for future clinical use of this technique.
SUMMARY
The contralateral somatosensory evoked responses to mechanical stimuli, such as pin-prick, touch and tactile tap, applied to the middle finger and to the big toe were studied in 33 normal young volunteers and in 61 patients with neurological disorders, with emphasis on the early components of the response. In normal subjects, the well-defined cortical responses to mechanical stimuli could be obtained by the method used in this study, but the consistency with which the responses could be recorded was a little lower than in the case of electrical stimulation. In each subject, the bilateral peak latencies and wave forms were almost equal,
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whereas the amplitudes were greatly changed over the two hemispheres The results obtained in this study with regard to a correlation between sensory defi-~ cit and alterations in the somatosensory evoked responses to mechanical stimulation in patients with peripheral neuropathy and with cerebral lesions are in general agreement with previous investigations of the responses evoked by electrical stimulation The findings in patients with dissociated sensory loss due to the spinal cord lesions suggest that the afferent impulses responsible for the somatosensory evoked responses to mechanical stimulation travel by the ventro-lateral tracts.
REFERENCES ALAJOUANINE,T., J. SCHERRER,J. BARBIZEI, J. CALVETAND R. VERLEY(1958) Potentiels evoqu6s corticaux chez des subjets atteints de troubles somesth6siques, Rev. neurol., 98: 757-761. DESMEDT, J. E., J. DEBECKERAND J. MANIt. (1965) Mise en 6vidence d'un signe 61ectrique cer6bral associ6 il la d+tection par le sujet, d'un stimulus sensoriel tactile, Bull. Acad. reed. belg., 5: 887-936. EHRENBERGER, K., P. FINKENZELLER, W. D. KEIDEL AND K. H. PI.ATTIG (1966) Elektrophysiologische Korrelation der Stevensschen Potenzfunktion und objektive Schwellenmessung am Vibrationssinn des Menschen, Pfliigers Arch. ges. PhysioL, 290: 114-123. FRANZ~N, O. AND K. OF~NLOCrt (1969) Evoked response correlates of psychophysical magnitude estimates for tactile stimulation in man, Exp. Brain Res, 8: 1--18. GmLIN, 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. HALLIDAY, A. M. AND A. A. MASON (1964) The effect of hypnotic anaesthesia on cortical responses, .L Neurol. Neurosurg. Psychiat., 27:300 312. HALLtDAV, A. M. AND G. S. WAKEHELD(1963) Cerebral evoked potentials in patients with dissociated sensory loss, J. Neurol. Neurosurg. Psychiat., 26:211 219. HRBEK, A., M. HRBKOVAAND H. G. LENARD (1968) Somatosensory evoked responses in newborn infants. Electroenceph. clin. Neurophysiol., 25: 443-448. LARSON. JR., S., J. SANCFS AND P. C. CttRtSFENSON (1966) Evoked somatosensory potentials m man Arch. NeuroL (Chic.), 15:88 93. LARSSON, L. E. AND T. S. PREVEC (1970) SoMArO-sensory response to mechanical stimulation as recorded in human EEG, Electroenceph. clin. NeurophysioL, 28: 162-172, MATSUMIYA,Y. AND D. I. MOSTOFSKY(1972) Somatosensory evoked responses elicited by corneal and nostril air puff stimulation, Electroenceph. clin. NeurophysioL, 33 : 225-227. MEYJES, JR., F. E. P. (1969) Some characteristics of the early components of the somato-sensory evoked response to mechanical stimuli in man. Psychiat. Neurol. Neurochir. (Amst), 72:263 268~ NAKANISHLT., K. TAKITAAND Y. TOYOKURA(1973) Somatosensory evoked responses to tactile tap in man, Electroenceph. clin. Neurophysiol., 3 4 : 1 6. WALTER,W. G. (1964) The convergence and interaction of visual, auditory, and tactile responses in human nonspecific cortex, Ann. N.Y. Acad. Sci., I 12: 320- 361. WILLIAMSON,P. D., W. R. GOFF ANt) T, ALLISON (1970) Somatosensory evoked responses in patients with unilateral cerebral lesions, Electroenceph. olin. NcurophysioL. 28 : 566 575.