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Short-latency somatosensory evoked potentials in myotonic dystrophy: Evidence for a conduction disturbance
Electroencephalograph)' and chmcal Neurophysiologv, 1985, 6 2 : 4 5 5 - 4 5 8
455
Elsevier Scientific Publishers Ireland, Ltd. S h o r t communication SHORT-LATENCY EVIDENCE
FOR
SOMATOSENSORY A CONDUCTION
EVOKED
DISTURBANCE
POTENTIALS
IN
MYOTONIC
DYSTROPHY:
i
P E G G Y S. G O T T 2 and D E A N S. K A R N A Z E
Department of Neurology, Los Angeles CounO,--University of Southern Cahfornia Medical Center, Los Angeles, CA 90033 (U.S.A.) (Accepted for publication: July 15, 1985)
Summary Short-latency somatosensory evoked potentials were recorded in 13 patients with myotonic dystrophy (MyD). The M y D were compared with age-matched controls. The mean conduction latency between the brachial plexus and dorsal column nuclei (EP-N14) was significantly longer for the MyD. Results suggest an afferent conduction disturbance in MyD.
Keywords: mvotonic dystrophy - short-latency SEPs
Myotonic dystrophy (MyD) is a multisystem disease once thought to be a primary degenerative disorder of muscle (Harper 1979). However, results from nerve conduction and somatosensory evoked potential (SEP) studies suggest some peripheral and central neural involvement (Caccia et al. 1972: Mongia and Lundervold 1975; Streib 1983; T h o m p s o n et al. 1983; Bartel et al. 1984). We previously reported abnormal pattern-shift visual evoked potentials in M y D (Gott et al. 1983). In an effort to gain further insight into the pathology of this disease and to determine if the posterior column mediated somatosensory pathway is affected in the same patients with visual evoked potential (VEP) abnormalities, we studied shortlatency somatosensory evoked potentials (SEPs) in 13 patients with documented MyD.
Methods
Patients Seven men and 6 women, age 19-57 years (mean 41.0), with confirmed myotonic dystrophy were studied. Eleven of the thirteen had been studied with pattern-shift VEPs. The duration since diagnosis of the disease was from 2 to 31 years. Severity of the disease ranged from mild (ambulatory) to severe (quadriplegia).
Normal subjects
tested 40 age-matched normal subjects (18 men, 22 women with an age range (19-55 years, mean 33.3) comparable to that of the patients.
Procedure All subjects were tested while lying supine in a quiet, semi-darkened, private room. A Nicolet Pathfinder II provided the stimulus and analysis for the SEPs. The stimulus was a 0.1 msec constant current electrical pulse applied to each median nerve independently at a rate of 5.1 Hz. Stimulus intensity was just sufficient to elicit a t h u m b twitch. One-thousand stimuli were averaged for a 50 msec epoch with 512 points. Montage for recording the SEP was Fz-EP, Fz-CII, Fz-Cc (EP = Erb's point, CII = second cervical vertebrae, Cc = 2 cm posterior to standard C 3 or C 4 on the hemisphere contralateral to the nerve stimulated). The amplifiers had a low cut-off of 30 Hz, a high cut-off of 1500 Hz, and amplification of 200,000. Latency measures were determined by cursors and the Pathfinder auto-program. A M A N O V A for latencies of waves EP, N14, P15, N19 and P22 showed a significant disease effect ( P ~< 0.05). The N l l peak was not included in the analysis since it was present in only 53% of the subjects (69% MyD, 47% controls). The significant M A N O V A controlled for type I errors, thus further a priori comparisons of differences between M y D and controls could be made by t tests for independent means without correction for multiple comparisons (Hummel and Sligo 1971).
To establish the normal mean and standard deviation for latency measures using the equipment of our laboratory, we
Results 1 We thank Drs. King Engel and Valerie Askanas for their assistance in obtaining the patients. 2 Address correspondence and reprint requests to Dr. Gott, LAC-USC Medical Center, Department of Neurology, General Hospital, R o o m 5641, 2025 Zonal Avenue, Los Angeles, CA 90033, U.S.A.
Means and S.D. for peak latencies and interpeak intervals are given in Table I. The N14 and N19 peak latency and EP-N14 interpeak were longer for the MyD. All other peak and interpeak latencies showed no significant difference between groups.
0168-5597/85/$03.30 © 1985 Elsevier Scientific Publishers Ireland, Ltd.
456
P.S. G O T T , D.S. K A R N A Z E
TABLE l
T A B L E II
M e a n peak and i n t e r p e a k latencies.
Visual evoked p o t e n t i a l P100 latencies.
Latency Myotonic dystrophy
Controls
Mean (msec)
S.D.
Mean (msec)
S.D.
10.4 12.9 14.4 17.0 19.8 22.5 4.0 6.7 9.3 12.1 5.4 8.1
0.67 1.04 0.76 0.75 0.92 1.46 0.56 0.61 0.82 1.30 0.65 1.27
9.9 12.4 13.6 16.7 19.2 22.1 3.6 6.7 9.2 12.1 5.6 8.5
0.79 1.08 0.97 1.04 1.00 1.08 0.44 0.56 0.53 0.81 0.41 0.73
Myotonic dystrophy
Controls
Mean (msec)
S.D.
Mean (msec)
S.D.
128 * 128 *
11.1 10.0
118 118
4.8 5.8
148 ** 149 **
17.0 23.2
122 122
6.6 6.6
Young age group EP Nll N 1 4 ** P15 NI9 * P22 E P - N 1 4 ** EP-P15 EP-NI9 EP-P22 N14-N19 N 14-P22
Left eye Right eye
Older age group Left eye R i g h t eye
t test, * P < 0.02, ** P < 0.001. Y o u n g age g r o u p = 2 0 - 3 9 years. O l d e r age group = 40 59 years.
t test, * P < 0.05, ** P < 0.01.
RIGHT MEDIA N
LEFT M E D I A N
NORMAL SUBJECT o"~ : Age 30
Fz - Cc
~
F z - CII /,~ ~
~ _
P22~~_~__=
Fz - EP
t
t MYOTONIC DYSTROPHY PATIENT
oJ: Age 19 N19
Fz -Cc
P22 N14
Fz -Cll Fz EP -
2 5F~V
t
Stimulus
Stimulus
,
5 rnsec
Fig. 1. M e d i a n nerve short-latency s o m a t o s e n s o r y evoked p o t e n t i a l s from a n o r m a l subject a n d a p a t i e n t w i t h m y o t o n i c dystrophy. E P = Erb's point; C I I = second cervical vertebrae; Cc = cortex c o n t r a l a t e r a l to side of s t i m u l a t i o n ; Fz = 10-20 system placement.
SEPs IN M Y O T O N I C D Y S T R O P H Y Representative SEP from a M y D patient and a control are given in Fig. 1. They were of comparable quality with well-defined peaks. The response of the M y D was representative of the patient group with peak and interpeak latencies within normal limits (normal upper limits = mean + 3 S.D.). Comparing results of the SEP with the previous VEP in patients who had both, 6 of l l patients had VEP measurements which exceeded normal limits. The only patient to show an SEP abnormality individually (EP-N14 at normal upper limit) had a normal VEP. As would be expected from the individual patient's data, the P100 peak latency was significantly longer for M y D as a group than for the controls (Table II).
Discussion lnterpeak conduction times, e.g., EP-N14, provide more valuable and conclusive information about the conduction in the somatosensory pathway than peak latencies. The EP-N14 and N14-N19 interpeak latencies are not correlated with conduction times in peripheral nerve while the N14 and N19 peak latencies are (Ganes 1980). Peripheral nerve transmission from SEPs can vary with age, room and limb temperature, and arm length, thus limiting its diagnostic value. The M y D patients had significantly longer EP-N14 interpeak latencies than controls. Delay of the N19 peak must be a result of the more caudal delay since N14-N19 interpeak latency was not different from controls. These results concur with those of Streib (1983) who also found the EP-N14 prolonged for the M y D group. However, T h o m p s o n et al. (1983) using a different recording montage found no group differences for M y D and controls, but two patients were reported to have a delay at the thalamic level. In contrast, slower peripheral conduction was reported for the M y D by Bartel et al. (1984). The group means for interpeak latencies and right-left interpeak differences were not statistically significant. Of the 33% of their patients with various abnormal findings, one had a delayed EP-N14 (his N9-N19) and one had an absent N14. The EP was not prolonged in any of our patients individually or in the M y D group compared with controls. The EP wave is thought to be generated by the ascending volley as it approaches and passes through the brachial plexus (Jones 1977: Hume and Cant 1978). The possible sources for the N14 include the root entry zone, dorsal column, dorsal column nucleus, and medial lemniscus (Desmedt and Cheron 1981: Lesser et al. 1981: Chiappa and Ropper 1982). With the Fz-CII derivation there are contributions to N14 from both electrodes: Fz positive and CII negative. The EP-N14 interpeak appears to reflect impulse propagation in the proximal plexus, the cervical roots, and the dorsal columns. The contribution of each of these components to the conduction time cannot be readily determined. There was a tendency for the interpeak latencies N14-N19 and N14-P22 to be shorter for the M y D than the controls. This observation is difficult to explain based on exclusive generation of the SEP in serial first order afferent fibers. However, it has
457 been proposed, but not proven, that SEP components are mediated through independent routes probably involving different first order fibers (Yamada et al. 1981). Also, compensatory mechanisms cannot be conclusively excluded. A possibly related observation was made with the brain-stem auditory evoked response in Guillain-Barr6 (Schiff et al. 1985). Two patients with prolonged l - I l l intervals had shortened I I I - V intervals. For the patients we tested, involvement of the central somatosensory system appeared less severe than the central visual system previously evaluated by VEP. Six of the 11 patients common to both studies had significantly prolonged VEP but with one exception, no individual abnormalities on the SEP. The SEP group differences suggest, however, a slowing in sensory conduction in M y D although the cause is yet uncertain. Together, these findings lead to the conclusion that M y D affects not only muscle but also the afferent sensory system. The evoked potential results suggest that this disorder may, in part, be neurogenic although we can not be certain whether the EP disturbances are related to pathogenesis or are simply part of a diffuse disease.
Resume Potentiels bvoqubs somatosensoriels h courte latence dans des cas de dystrophie myotonique: arguments en faveur d'une perturbation de la conduction Des potentiels 6voqu6s h courte latence ont 6t6 enregistr6s chez 13 patients pr6sentant une dystrophie myotonique (DMy). Ces patients ont 6t6 compar6s/t des t6moins d'~tge correspondant. La latence moyenne de conduction entre le plexus brachial et les noyaux de la colonne dorsale (EP-N14) 6tait significativement plus longue chez les DMy. Ces r6sultats sugg6rent une perturbation de la conduction des aff6rences dans la DMy.
References Bartel, P.R., Lotz, B.P. and Van der Meyden, C.H. Short-latency somatosensory evoked potentials in dystrophia myotonica. J. Neurol. Neurosurg. Psychiat., 1984, 47: 524-529. Caccia, M.R., Negri, S. and Parvis, V.P. Myotonic dystrophy with neural involvement. J. neurol. Sci., 1972, 16: 253-269. Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1205-1211. Desmedt, J.E. and Cheron, G. Prevertebral (oesphageal) recording of subcortical somatosensory evoked potentials in man: the spinal PI3 component and the dual nature of spinal generators. Electroenceph. clin. Neurophysiol, 1981, 52: 257-275. Ganes, T. A study of peripheral, cervical, and cortical evoked potentials and afferent conduction times in the somatosensory pathway. Electroenceph. clin. Neurophysiol., 1980, 49: 446-451.
458 Gott, P.S., Karnaze, D.S. and Keane, J.R. Abnormal visual evoked potentials in myotonic dystrophy. Neurology (NY), 1983, 33: 1622-1625. Harper, P.S. Myotonic dystrophy. Saunders, Philadelphia, PA, 1979. Hume, A.L. and Cant, B.R. Conduction time in central somatosensory pathways in man. Electroenceph. clin. Neurophysiol., 1978, 45:361 375. Hummel, T.J. and Sligo, J.R. Empirical comparison of univariate and multivariate analysis of variance procedures. Psychol. Bull., 1971, 76: 49-57. Jones, S.J. Short latency potentials recorded from the neck and scalp following median nerve stimulation in man. Electro° enceph, clin. Neurophysiol., 1977, 43: 853-863. Lesser, R.P., Lueders, H., Hahn, J. and Klem, G. Early somatosensory potentials evoked by median nerve stimulation: intraoperative monitoring. Neurology (Minneap.), 1981, 31: 1519-1523.
P.S. GO'IT, D.S. KARNAZE Mongia, S.K. and Lundervold, A. Electrophysiological abnormalities in cases of dystrophia myotonica. Europ. Neurol., 1975, 13: 360-376. Schiff, J.A., Cracco, R.Q. and Cracco, J.B. Brainstem auditory evoked potentials in Guillain-Barr6 syndrome. Neurology (NY), 1985, 35: 771-773. Streib, E.W. Somatosensory evoked responses (SSER) in myotonic muscular dystrophy (MyD). Electroenceph. olin. Neurophysiol., 1983, 56: 178. Thompson, D.S., Woodward, J.B., Ringel, S.P. and Nelson, L.M. Evoked potential abnormalities in myotonic dystrophy. Electroenceph. clin. Neurophysiol., 1983, 56: 453-456. Yamada, T., Muroga, T. and Kimura, J. Tourniquet-induced ischemia and somatosensory evoked potentials. Neurology (Minneap.), 1981, 31: 1524-1529.
455
Elsevier Scientific Publishers Ireland, Ltd. S h o r t communication SHORT-LATENCY EVIDENCE
FOR
SOMATOSENSORY A CONDUCTION
EVOKED
DISTURBANCE
POTENTIALS
IN
MYOTONIC
DYSTROPHY:
i
P E G G Y S. G O T T 2 and D E A N S. K A R N A Z E
Department of Neurology, Los Angeles CounO,--University of Southern Cahfornia Medical Center, Los Angeles, CA 90033 (U.S.A.) (Accepted for publication: July 15, 1985)
Summary Short-latency somatosensory evoked potentials were recorded in 13 patients with myotonic dystrophy (MyD). The M y D were compared with age-matched controls. The mean conduction latency between the brachial plexus and dorsal column nuclei (EP-N14) was significantly longer for the MyD. Results suggest an afferent conduction disturbance in MyD.
Keywords: mvotonic dystrophy - short-latency SEPs
Myotonic dystrophy (MyD) is a multisystem disease once thought to be a primary degenerative disorder of muscle (Harper 1979). However, results from nerve conduction and somatosensory evoked potential (SEP) studies suggest some peripheral and central neural involvement (Caccia et al. 1972: Mongia and Lundervold 1975; Streib 1983; T h o m p s o n et al. 1983; Bartel et al. 1984). We previously reported abnormal pattern-shift visual evoked potentials in M y D (Gott et al. 1983). In an effort to gain further insight into the pathology of this disease and to determine if the posterior column mediated somatosensory pathway is affected in the same patients with visual evoked potential (VEP) abnormalities, we studied shortlatency somatosensory evoked potentials (SEPs) in 13 patients with documented MyD.
Methods
Patients Seven men and 6 women, age 19-57 years (mean 41.0), with confirmed myotonic dystrophy were studied. Eleven of the thirteen had been studied with pattern-shift VEPs. The duration since diagnosis of the disease was from 2 to 31 years. Severity of the disease ranged from mild (ambulatory) to severe (quadriplegia).
Normal subjects
tested 40 age-matched normal subjects (18 men, 22 women with an age range (19-55 years, mean 33.3) comparable to that of the patients.
Procedure All subjects were tested while lying supine in a quiet, semi-darkened, private room. A Nicolet Pathfinder II provided the stimulus and analysis for the SEPs. The stimulus was a 0.1 msec constant current electrical pulse applied to each median nerve independently at a rate of 5.1 Hz. Stimulus intensity was just sufficient to elicit a t h u m b twitch. One-thousand stimuli were averaged for a 50 msec epoch with 512 points. Montage for recording the SEP was Fz-EP, Fz-CII, Fz-Cc (EP = Erb's point, CII = second cervical vertebrae, Cc = 2 cm posterior to standard C 3 or C 4 on the hemisphere contralateral to the nerve stimulated). The amplifiers had a low cut-off of 30 Hz, a high cut-off of 1500 Hz, and amplification of 200,000. Latency measures were determined by cursors and the Pathfinder auto-program. A M A N O V A for latencies of waves EP, N14, P15, N19 and P22 showed a significant disease effect ( P ~< 0.05). The N l l peak was not included in the analysis since it was present in only 53% of the subjects (69% MyD, 47% controls). The significant M A N O V A controlled for type I errors, thus further a priori comparisons of differences between M y D and controls could be made by t tests for independent means without correction for multiple comparisons (Hummel and Sligo 1971).
To establish the normal mean and standard deviation for latency measures using the equipment of our laboratory, we
Results 1 We thank Drs. King Engel and Valerie Askanas for their assistance in obtaining the patients. 2 Address correspondence and reprint requests to Dr. Gott, LAC-USC Medical Center, Department of Neurology, General Hospital, R o o m 5641, 2025 Zonal Avenue, Los Angeles, CA 90033, U.S.A.
Means and S.D. for peak latencies and interpeak intervals are given in Table I. The N14 and N19 peak latency and EP-N14 interpeak were longer for the MyD. All other peak and interpeak latencies showed no significant difference between groups.
0168-5597/85/$03.30 © 1985 Elsevier Scientific Publishers Ireland, Ltd.
456
P.S. G O T T , D.S. K A R N A Z E
TABLE l
T A B L E II
M e a n peak and i n t e r p e a k latencies.
Visual evoked p o t e n t i a l P100 latencies.
Latency Myotonic dystrophy
Controls
Mean (msec)
S.D.
Mean (msec)
S.D.
10.4 12.9 14.4 17.0 19.8 22.5 4.0 6.7 9.3 12.1 5.4 8.1
0.67 1.04 0.76 0.75 0.92 1.46 0.56 0.61 0.82 1.30 0.65 1.27
9.9 12.4 13.6 16.7 19.2 22.1 3.6 6.7 9.2 12.1 5.6 8.5
0.79 1.08 0.97 1.04 1.00 1.08 0.44 0.56 0.53 0.81 0.41 0.73
Myotonic dystrophy
Controls
Mean (msec)
S.D.
Mean (msec)
S.D.
128 * 128 *
11.1 10.0
118 118
4.8 5.8
148 ** 149 **
17.0 23.2
122 122
6.6 6.6
Young age group EP Nll N 1 4 ** P15 NI9 * P22 E P - N 1 4 ** EP-P15 EP-NI9 EP-P22 N14-N19 N 14-P22
Left eye Right eye
Older age group Left eye R i g h t eye
t test, * P < 0.02, ** P < 0.001. Y o u n g age g r o u p = 2 0 - 3 9 years. O l d e r age group = 40 59 years.
t test, * P < 0.05, ** P < 0.01.
RIGHT MEDIA N
LEFT M E D I A N
NORMAL SUBJECT o"~ : Age 30
Fz - Cc
~
F z - CII /,~ ~
~ _
P22~~_~__=
Fz - EP
t
t MYOTONIC DYSTROPHY PATIENT
oJ: Age 19 N19
Fz -Cc
P22 N14
Fz -Cll Fz EP -
2 5F~V
t
Stimulus
Stimulus
,
5 rnsec
Fig. 1. M e d i a n nerve short-latency s o m a t o s e n s o r y evoked p o t e n t i a l s from a n o r m a l subject a n d a p a t i e n t w i t h m y o t o n i c dystrophy. E P = Erb's point; C I I = second cervical vertebrae; Cc = cortex c o n t r a l a t e r a l to side of s t i m u l a t i o n ; Fz = 10-20 system placement.
SEPs IN M Y O T O N I C D Y S T R O P H Y Representative SEP from a M y D patient and a control are given in Fig. 1. They were of comparable quality with well-defined peaks. The response of the M y D was representative of the patient group with peak and interpeak latencies within normal limits (normal upper limits = mean + 3 S.D.). Comparing results of the SEP with the previous VEP in patients who had both, 6 of l l patients had VEP measurements which exceeded normal limits. The only patient to show an SEP abnormality individually (EP-N14 at normal upper limit) had a normal VEP. As would be expected from the individual patient's data, the P100 peak latency was significantly longer for M y D as a group than for the controls (Table II).
Discussion lnterpeak conduction times, e.g., EP-N14, provide more valuable and conclusive information about the conduction in the somatosensory pathway than peak latencies. The EP-N14 and N14-N19 interpeak latencies are not correlated with conduction times in peripheral nerve while the N14 and N19 peak latencies are (Ganes 1980). Peripheral nerve transmission from SEPs can vary with age, room and limb temperature, and arm length, thus limiting its diagnostic value. The M y D patients had significantly longer EP-N14 interpeak latencies than controls. Delay of the N19 peak must be a result of the more caudal delay since N14-N19 interpeak latency was not different from controls. These results concur with those of Streib (1983) who also found the EP-N14 prolonged for the M y D group. However, T h o m p s o n et al. (1983) using a different recording montage found no group differences for M y D and controls, but two patients were reported to have a delay at the thalamic level. In contrast, slower peripheral conduction was reported for the M y D by Bartel et al. (1984). The group means for interpeak latencies and right-left interpeak differences were not statistically significant. Of the 33% of their patients with various abnormal findings, one had a delayed EP-N14 (his N9-N19) and one had an absent N14. The EP was not prolonged in any of our patients individually or in the M y D group compared with controls. The EP wave is thought to be generated by the ascending volley as it approaches and passes through the brachial plexus (Jones 1977: Hume and Cant 1978). The possible sources for the N14 include the root entry zone, dorsal column, dorsal column nucleus, and medial lemniscus (Desmedt and Cheron 1981: Lesser et al. 1981: Chiappa and Ropper 1982). With the Fz-CII derivation there are contributions to N14 from both electrodes: Fz positive and CII negative. The EP-N14 interpeak appears to reflect impulse propagation in the proximal plexus, the cervical roots, and the dorsal columns. The contribution of each of these components to the conduction time cannot be readily determined. There was a tendency for the interpeak latencies N14-N19 and N14-P22 to be shorter for the M y D than the controls. This observation is difficult to explain based on exclusive generation of the SEP in serial first order afferent fibers. However, it has
457 been proposed, but not proven, that SEP components are mediated through independent routes probably involving different first order fibers (Yamada et al. 1981). Also, compensatory mechanisms cannot be conclusively excluded. A possibly related observation was made with the brain-stem auditory evoked response in Guillain-Barr6 (Schiff et al. 1985). Two patients with prolonged l - I l l intervals had shortened I I I - V intervals. For the patients we tested, involvement of the central somatosensory system appeared less severe than the central visual system previously evaluated by VEP. Six of the 11 patients common to both studies had significantly prolonged VEP but with one exception, no individual abnormalities on the SEP. The SEP group differences suggest, however, a slowing in sensory conduction in M y D although the cause is yet uncertain. Together, these findings lead to the conclusion that M y D affects not only muscle but also the afferent sensory system. The evoked potential results suggest that this disorder may, in part, be neurogenic although we can not be certain whether the EP disturbances are related to pathogenesis or are simply part of a diffuse disease.
Resume Potentiels bvoqubs somatosensoriels h courte latence dans des cas de dystrophie myotonique: arguments en faveur d'une perturbation de la conduction Des potentiels 6voqu6s h courte latence ont 6t6 enregistr6s chez 13 patients pr6sentant une dystrophie myotonique (DMy). Ces patients ont 6t6 compar6s/t des t6moins d'~tge correspondant. La latence moyenne de conduction entre le plexus brachial et les noyaux de la colonne dorsale (EP-N14) 6tait significativement plus longue chez les DMy. Ces r6sultats sugg6rent une perturbation de la conduction des aff6rences dans la DMy.
References Bartel, P.R., Lotz, B.P. and Van der Meyden, C.H. Short-latency somatosensory evoked potentials in dystrophia myotonica. J. Neurol. Neurosurg. Psychiat., 1984, 47: 524-529. Caccia, M.R., Negri, S. and Parvis, V.P. Myotonic dystrophy with neural involvement. J. neurol. Sci., 1972, 16: 253-269. Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1205-1211. Desmedt, J.E. and Cheron, G. Prevertebral (oesphageal) recording of subcortical somatosensory evoked potentials in man: the spinal PI3 component and the dual nature of spinal generators. Electroenceph. clin. Neurophysiol, 1981, 52: 257-275. Ganes, T. A study of peripheral, cervical, and cortical evoked potentials and afferent conduction times in the somatosensory pathway. Electroenceph. clin. Neurophysiol., 1980, 49: 446-451.
458 Gott, P.S., Karnaze, D.S. and Keane, J.R. Abnormal visual evoked potentials in myotonic dystrophy. Neurology (NY), 1983, 33: 1622-1625. Harper, P.S. Myotonic dystrophy. Saunders, Philadelphia, PA, 1979. Hume, A.L. and Cant, B.R. Conduction time in central somatosensory pathways in man. Electroenceph. clin. Neurophysiol., 1978, 45:361 375. Hummel, T.J. and Sligo, J.R. Empirical comparison of univariate and multivariate analysis of variance procedures. Psychol. Bull., 1971, 76: 49-57. Jones, S.J. Short latency potentials recorded from the neck and scalp following median nerve stimulation in man. Electro° enceph, clin. Neurophysiol., 1977, 43: 853-863. Lesser, R.P., Lueders, H., Hahn, J. and Klem, G. Early somatosensory potentials evoked by median nerve stimulation: intraoperative monitoring. Neurology (Minneap.), 1981, 31: 1519-1523.
P.S. GO'IT, D.S. KARNAZE Mongia, S.K. and Lundervold, A. Electrophysiological abnormalities in cases of dystrophia myotonica. Europ. Neurol., 1975, 13: 360-376. Schiff, J.A., Cracco, R.Q. and Cracco, J.B. Brainstem auditory evoked potentials in Guillain-Barr6 syndrome. Neurology (NY), 1985, 35: 771-773. Streib, E.W. Somatosensory evoked responses (SSER) in myotonic muscular dystrophy (MyD). Electroenceph. olin. Neurophysiol., 1983, 56: 178. Thompson, D.S., Woodward, J.B., Ringel, S.P. and Nelson, L.M. Evoked potential abnormalities in myotonic dystrophy. Electroenceph. clin. Neurophysiol., 1983, 56: 453-456. Yamada, T., Muroga, T. and Kimura, J. Tourniquet-induced ischemia and somatosensory evoked potentials. Neurology (Minneap.), 1981, 31: 1524-1529.