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Diagnostic recording of somato-sensory cortical evoked potentials in man
260
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
AND
LABORATORY
NOTES
DIAGNOSTIC RECORDING OF SOMATO-SENSORY CORTICAL EVOKED POTENTIALS IN M A N L. BERGAMINI, B. BERGAMASCO, L. FRA, G . GANDIGLIO AND R . MUTANI
Neurological Clinic, University of Turin, Turin (Italy) (Accepted for publication: September 7, 1966)
The study in man by integration techniques of the response elicited in the specific cortical area by contralateral somaesthetic stimulation (electrical stimulation of a nerve) may be of considerable clinical importance. Significant data for diagnostic purposes have already been recorded by this technique in peripheral and spinal nerve lesions (Alajouanine et al. 1958; Halliday and Wakefield 1963; Giblin 1964; Bergamini et al. 1965, 1967). This report deals with an unusual diagnostic application of this neurophysiological technique in a pair of female Siamese twins who were studied before successful surgical division. CASE The two dorsally-linked, 6-year-old, Siamese female twins presented a very rare abnormality (incidence of about one in 300,000 newborns). The junction involved the gluteal soft parts, the sacrum and coccyx, with fusion of rectal and urogenital terminal parts (anus and vagina in common). They had been followed in the Pediatric Clinic of Turin University from their birth until their separation: complete details have been described by Gomirato-Sandrucci et aL (1966). A neurophysiological investigation was requested before surgery to determine, if possible, the absolute independence of their peripheral nervous pathways, since they had a vertebral segment in common. The idea of a possible common sacral or lumbosacral peripheral nervous pathway was supported: (1) by the fusion of the sacral spinal colurfffi; (2) by the presence of marked atrophy of the medial surface of the thigh muscles of the "internal" limbs, which is dorsally visible (Fig. 1) in the right lower limb in the left twin and in the left lower limb in the right twin; (3) by the dubious results of clinical examination of the general sensitivity and of the reflexes. In fact, due to the psychological condition provoked by years of Siamese life, surface sensory stimuli and proprioceptive tapping on the leg of one twin sometimes seemed to produce a remarkable response in the other twin. On the contrary, favouring independent nervous systems of the sisters was the consideration that the vertebral
fusion was too low to involve nerve roots immediately at their exits from the intervertebral foramina. At the surgeon's request for a detailed neurophysiological investigation to clarify any doubts concerning the presence of common peripheral nerve fibres, we decided to utilize the somato-sensory cortical evoked potential. If there were even minimal common lumbo-sacral peripheral nerves, stimulating a nerve in one twin's lower limb should produce an evoked response in the somaesthetic cortical area of the other twin. METHOD The lateral popliteal nerves at the heads of the fibulae of the twins' four lower limbs were stimulated by supramaximal electrical shocks with a 0.5/sec frequency, delivered from a constant current stimulator through surface electrodes. Recordings (4 channels) were made simultaneously of the activity evoked from the contralateral and ipsilateral somaesthetic areas with regard to the stimulated limb, and from both somaesthetic cortical areas of the other twin. The electrodes were placed on the cranial projection of the "leg" cortical area according to Kr6nlein (1898). The evoked somato-sensory responses were recorded with bipolar connections from the scalp and were averaged by means of a CAT 400 B (Mnemotron Corp.). The E E G was always simultaneously recorded. Two to three hundred cortical responses were averaged in order to detect even the smallest evoked potential. H reflex investigation with an E M G apparatus was also performed in all four limbs. This consisted in submaximal stimulation of the posterior tibial nerve in the popliteal fossa of one limb and detection of the motor reflex response in the sural triceps of each of the four limbs. RESULTS The response evoked in the post-Rolandic area to somaesthetic stimulation of a contralateral lower limb of each subject was always individual and physiological (Fig. 1). In other words, no activity recorded from the subject's scalp was ever found in the twin whose lateral popliteal nerve was not simultaneously stimulated on the opposite side.
Electroenceph. clin. Neurophysiol., 1967, 22:260-262
26l
SOMATO-SENSORY EVOKED POTENTIALS IN MAN
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Fig. 1 Cortical somato-sensory potentials evoked by stimulating the lateral popliteal nerves at the heads of the fibulae of the twins (A-B-C-D) with supramaximal rectangular electrical pulses at a frequency of 0.5/sec (average of 250 cortical potentials). For each stimulation site the evoked potentials were simultaneously recorded from the 4 postRolandic areas of the twins. When a nerve of one twin was stimulated, a normal evoked potential was seen only in her contralateral post-Rolandic area. In the ipsilateral area later low voltage waves occurred. In the somaesthetic areas of the twin whose nerve was not stimulated, no evoked activity was seen. For example, when stimulating Gius.'s right nerve (A), there is a normal cortical evoked potential only in Gius.'s left somaesthetic area (1) and later components in her right area (r), while in Sant.'s 2 areas (r and l) no evoked activity is recorded. In addition, the H reflex investigation showed identical latencies in all the limbs (between 20.4 and 21.2 msec) and the presence of reflex responses always only in the stimulated limb. Therefore it was possible to conclude that there were no common spinal sensory pathways in the twins. This conclusion was confirmed by surgery (Solerio 1965), which successfully led to a normal and independent life for the twins. SUMMARY In a pair of Siamese twins joined by lumbo-sacral spinal column fusion, the somato-sensory cortical evoked potentials were used to determine the complete independence of the spinal sensory fibres. Stimulation of one twin's lateral popliteal nerve never provoked cortical responses recordable from the other's scalp. In addition, the H reflex was always obtained only in the stimulated limb. Surgery later confirmed the complete independence of the twins' peripheral nervous systems. RI~SUM]~ ENREGISTREMENT DIAGNOSTIQUE DU POTENTIEL EVOQUI~ SOMESTHI~SIQUE CHEZ L'HOMME Chez des j umelles conjointes pygopages avec fusion de
la colonne lombo-sacr6e, l'enregistrement du potentiel cortical 6voqu6 somesth6sique a 6t6 eraploy6 pour d6terminer la complete ind6pendance des fibres nerveuses spinales sensitives. La stimulation du nerf sciatique poplit6 exter•e d'une jumelle n'a jamais donn6e une r6ponse corticale enregistrable sur le cuir chevelu de l'autre jumelle. En outre, le r6flexe H n'a jamais 6t6 obtenu en dehors du membre inf6rieur stimul6. L'intervention chirurgicale a confirm6 la complete ind6pendance des syst~mes nerveux p6riph6riques des jumelles.
REFERENCES BARBIZET, J., CALVET, J. et VERLEY,R. Potentiels 6voqu6s corticaux chez des sujets atteints de troubles somesth6siques. Rev. neurol., 1958, 98: 757-761. BERGAMINI, L., BERGAMASCO, l . , FRA, L., GANDIGLIO, G., MOMBELLI,A. M. and MUTANI, R. Somato-sensory evoked cortical potentials in subjects with peripheral nervous lesions. Electromyography, 1965, 5: 121-130. BERGAMINI, L., BERGAMASCO, B., FRA, L., GANDIGLIO, G., MOMBELLI, A. M. et MUTANI, R. R6ponses corticales et p6riph6riques 6voqu6es par stimulation du ALAJOUANINE, T . , SCHERRER, J.,
Electroenceph. clin. Neurophysiol., 1967, 22:260-262
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nerf dans la pathologie des cordons post6rieurs. Rev. neurol., 1967, in press. GIBLIN,D. R. Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann. N. Y. Acad. Sci., 1964, 112: 93-141. GOMIRATO-SANDRUCCI,M., MUSSA, G. C. e MARCHESE, G. S. I gemelli siamesi (illustrazione di una coppia di gemelle pigopaghe). Minerva pediat., 1966, 18:11211150.
HALLIDAY,A. M. and WAKEFIELD, G. S. Cerebral evoked potentials in patients with dissociated sensory loss. J. NeuroL Neurosurg. Psychiat., 1963, 26: 211-219. KR()NLEIN, R. U. Ztlr cranio-cerebralen Topographie. Beitr. klin. Chirurg., 1898, 22: 364-370. SOLERIO, L. Separazione di due gemelle congiunte pigopaghe (nota preventiva). Minert,a reed., 1965, 56: 1-4.
Reference: BERGAMINI,L., BERGAMASCO,B., FRA, L., GANDIGLIO,G. and MUTANI,R. Diagnostic recording of somatosensory cortical evoked potentials in man. Electroenceph. clin. Neurophysiol., 1967, 22: 260-262.
OBSERVATIONS
ON HIGH FREQUENCY
ELECTROENCEPHALOGRAMS 1 R . A . HALL, M . D . , C. YEAGER, M . D . AND R . B. YARBROUGH, P H . D .
Psychophysiological Research Laboratory, Institute for Medical Research of Santa Clara County, San Jose, Calif. (U.S.A.) (Accepted for publication: August 31, 1966) INTRODUCTION From the point of view of information theory, to obtain all the information contained in a signal, all frequency components present must be examined (Schwartz 1959). Therefore, to obtain additional information about the brain from its transmitted electrical potentials, all frequency components should be studied. This report considers activity up to 250 c/sec. It would appear that technical rather than theoretical reasons have, in the past, limited study of the E E G signal to frequency components from about 1 to 50 c/sec. The lower limit appears to have been set by problems of electrode polarization and the instability of early D C amplifiers. Recent work by Goldring and O'Leary (1951) on steady potentials has shown that valuable information is obtainable from the EEG signal by extending the lower frequency limit. Study of higher frequencies seems to have been restricted by the physical capabilities of the inkwriting oscillograph. Mostly using cathode ray oscillography, a number of workers have looked at the higher frequencies beginning with Gozzano (1935). Adrian (1935) reported frequencies above 200 c/sec from the cerebellum. According to Drohocki (1945), the existence of frequencies up to 200 c/sec of cerebral (and non-muscular) origin is incontestable. Recording from the h u m a n scalp and exposed cat cortex, Lion et al. (1950) found potentials up to 70/~V in the 200-1400 c/sec range. Recording a rectified presentation 1 This work was supported, in part, by a grant from the Scottish Rite Committee for Research in Schizophrenia.
of components in the 100-13,000 c/sec range from implanted depth electrodes in the cat brain, Schlag and Balvin (1963) reported that this "background activity" varies with probe location and shows high correlation with and often prediction of changes in standard EEG. Baumann et al. (1964) reported activity up to 5800 c/sec using depth probes in animal brains. Schwarzer (1949) described an E E G machine employing a stylus and carbon-paper method which produces records having a fiat response up to 200 c/sec. However, we have found no reports of the application of this machine to study of high frequency EEG. The same applies to II'ianok's (.1960) modification of the Grey Walter harmonic analyzer which extends its range to 480 c/sec. The present report describes a method of obtaining paper records of "fast E E G " (FEEG) free of the lower frequencies which characterize the "'standard E E G " (SEEG). Sample records are presented along with findings from the study of many such traces. METHOD Beckman electrodes 2 were applied at Fp~, C3 and O1, according to the International 10-20 System. The signal source of channel I was Fp~ and C3 and for channel It was C3 and O1. A negative potential on Cz produces a downward pen-deflection in channel I and an upward deflection in channel II. The specially built Cemco amplifiers 3 have an input impedance of 200 kf2 and selectable band passes of 50-250 c/sec or 1-50 c/sec with 12 db per octave roll-off produced by active filters. Maximum peak 2 Beckman Instruments Co., Palo Alto, Calif. California Electronics Manufacturing Co., Alamo, Calif.
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; IOOms~ Fig. 1 S a m p l e t r a c e s o f F E E G a n d B E E G . A l l E E G t r a c e s are F E E G e x c e p t B E E G i n first a n d s e c o n d t r a c e s o f ( A ) a n d third a n d f o u r t h t r a c e s in ( F ) . T i m e c a l i b r a t i o n o f 100 m s e c at t o p a n d b o t t o m a p p l y to all t r a c e s e x c e p t t h o s e in (C). T r a c e s (A) t h r o u g h ( E ) are f r o m a 4 2 - y e a r - o l d f e m a l e : (A) basal state traces, (B) b a s a l state F E E G 1 m i n later, ( C ) C R O p h o t o g r a p h s o f w h i c h left is 10 k c n o i s e , o t h e r s are F E E G at a b o u t s a m e t i m e as ( B ) , ( D ) t r a c e s o n a n o t h e r day, a n d ( E ) t r a c e s w h i l e r e a d i n g . T r a c e s m ( F ) are f r o m a 3 8 - y e a r - o l d f e m a l e u n d e r lateral eye m o t i o n , first left a n d t h e n right, o n v o i c e c o m m a n d s r e c o r d e d in b o t t o m trace.
R . A . HALL et al.
264
to peak noise in the higher band pass is 2 # V with shorted input and 4.8/zV with a 10 kf~ input resistor. To show the simultaneous relationship between F E E G and SEEG, the unfiltered Cemco pre-amplifier output was led (in 4 cases) into Tektronix 122 pre-amplifiers set at a band pass of 0.2-250 c/sec, yielding " b r o a d band E E G " (BEEG). All signals were recorded on magnetic tape with a Precision Instruments Co. Model PS 207A F M systemL Paper records were made off-line on a Model 6 Grass E E G machine 2, with taped signal played at half speed. This yielded oscillographic records of the F E E G with the 3 db frequency point thus raised from the usual 70 c/sec to 140 c/sec and with attenuation of the frequencies below 50 c/sec (about --30 db for the alpha activity). Recordings were made in a moderately illuminated and grounded Faraday Cage. Subjects were fourteen normal persons, half of each sex, ranging from 26 to 61 years of age. None had a history of epilepsy, of abnormal EEG, or of taking any medication for at least 7 da}s, aside from aspirin and insulin (by one diabetic woman). All were right-handed. A recording in a relaxed basal state with eyes closed (BS) was takenfrom thirteen subjects. The usual procedure was to first record the F E E G for 10 min and then the SEEG for 5 min. However, in four cases B E E G and F E E G were recorded simultaneously for 10 min, In ten subjects a 5 min sample with eyes open was also taken, always prior to the basal state record, and in one subject this constituted the entire record. Records were obtained from three subjects performing lateral and vertical eye movements on voice command which was recorded simultaneously with B E E G and FEEG. A record was taken from one subject while reading in order to show the effects of muscular artifacts. The results reported here are derived from visual study of the entire ink-written records. All parameters were quantified as far as possible. All SEEGs and BEEGs were interpreted to be normal in regard to the lower frequency patterns. Maximum amplitude was taken as the largest peak to peak voltage. Average amplitude was estimated by scanning the entire record to obtain a mean level. Frequency estimations were made by a combination of counting waves per unit time and measuring periods. Statistical measures were based on the assumption of a normal population. The student t statistic was used in all cases.
RESULTS
General The F E E G records varied considerably from subject to subject, whereas for any given subject the Fpl-C8 and C8-O1 wave patterns appeared to be similar. With simultaneous recording of F E E G and B E E G no consistent relationship was observed between particular F E E G waves (such as the "spikes" to be described below) and the slow waves. Precision Instruments Co., Palo Alto, Calif. 2 Grass Instrument Co., Quincy, Mass.
Sample records In Fig. 1, A the F E E G records show typical high frequency activity. The mean amplitudes in Fpl-Ca and C~-O1 are 10 and 6/zV respectively (noise level: 3/~V). The frequency range, excluding "spikes", is from 50 to 120 c/sec. The peak amplitude of about 2 5 / t V is contributed by "spikes" occurring at a rate of about 20/sec. These are predominantly synchronous in the two derivations with opposing polarities. While the "spiking" appears in both F E E G and BEEG records, there is no obvious correlation between the alpha wave form and the FEEG. In B, the "spiking" activity is similar but of smaller amplitude. (See legend for further explanations.) The record E (taken while this subject was reading) shows the difference between bursts of large amplitude muscular artifacts and the ongoing F E E G in Fpl-Ca; the smaller amplitude portion contains activity similar to that of the basal state, while the muscular activity is characterized by periods of 3-10 msec per phase. The Ca-O~ derivation remains unaffected by the muscle contraction, but still shows ongoing high frequency waves. The records in F are from another subject performing lateral eye movements. In both the F E E G and B E E G traces of Fp~-Ca triphasic waves with phase periods of 7-18 msec are observed, apparently initiating the slower transient in the BEEG trace.
Measurements I. Amplitude. Measurements were made of F E E G records (obtained during the eyes open condition) for both Fpl-C3 and C~-O1, in ten subjects for a total of 20 measurements each of average and maximum voltage. Similar measurements of BS F E E G records were made in thirteen subjects for a total of 26 measurements each of average and maximum voltages. The mean of the 46 average measurements was 8.3/~V (range 4-20 #V) and the mean of the maximum measurements was 23.4/~V (range 7-90/~V). The 23 FpI-C8 traces showed a mean for average voltage measurements of 9.6/~V as compared to 7.0 #V for the 23 C8-O1 traces, a difference that is not statistically significant ( P : 0.1). The mean of 14 BS measurements of average F E E G voltage in seven females was 10.6/~V as compared to 6.0 pV for 12 measurements insix males, a difference significant at the 2 % level. Examination of both average and maximum measurements of the anterior F E E G failed to demonstrate any significant difference between the eyes open and basal state. Positive correlations ( P = 0.05) were found between the F p l - C s basal state SEEG (or BEEG) maximum amplitude and both the maximum F E E G amplitudes (in both conditions) in FpI-C3 and C3-O1. Significant (P = 0.05) correlations were found between all F E E G maximum amplitudes, and between all F E E G average amplitudes except for the correlation between eyes open in Fpl-Ca and basal state in C8-O1. II. Frequency. Frequencies ranging up to 200 c/sec were observable in the records, sometimes in runs of about 5 waves of up to 10/zV amplitude at the upper frequency
Electroenceph. clin. Neurophysiol., 1967, 22:262-265
HIGH FREQUENCY EEG limit. Dominant rhythmicities of 80-100 c/sec were often seen. The mean of highest observable frequencies in 23 anterior traces was 139 c/sec and for 22 posterior traces was 120 c/sec, a difference which is not significant (P = 0.2). Ill. Morphology. The "spiking", triphasic waves of about 30 msec total duration, were the only obvious wave form characteristic of the F E E G and were regularly observed in all records. They tended to be synchronous in Fpl-C3 and C3-O1, with opposite or same polarity. Their rate of occurrence would range from 7 to 20/sec, occasionally reaching 40/sec. DISCUSSION The records of muscle artifact and directed eye movement showed periods similar to the F E E G "spiking". Considering this and the fact that the frequency range of the F E E G and that of muscular contractions (see Kaiser and Peters6n 1963) overlap, the question of E M G origin of much of the F E E G must be raised. This is particularly true for anterior derivations where muscle potentials are commonly present in the standard EEG (see Mark 1947). The trend toward higher potentials in Fpl-C3 is consistent with this possibility. However, the F E E G during eyes open, in which we might expect more muscular potentials anteriorly, showed no significant difference from the F E E G of the basal state. A common brain signal source is suggested by the amplitude correlations between the basal anterior SEEG and the FEEG. The "spiking" potentials strikingly resemble Trabka's (1962) examples of sensory evoked high frequency potentials in the cortex of the Nembutalized cat, suggesting brain origin of at least this component of the FEEG. Regularly obtaining these "spiking" F E E G records from normal subjects suggests that they may be a normal neurophysiological phenomenon. SUMMARY EEG potentials from the dominant hemisphere of fourteen normal persons were recorded on magnetic tape with high (50-250 c/see) and low (1-50 c/sec) or broad (0.2-250 c/see) band pass filtering. Write-out was obtained from a standard EEG machine with the taped signal played at half speed. This yielded an oscillographic record of the filtered "fast E E G " (FEEG) freed of effects of the lower frequencies. In the eyes-closed resting state FEEG-, the group mean of average amplitude was 8.3 ~V and the mean of maximum amplitudes was 23.4 #V. The amplitudes showed a correlation between F E E G and standard EEG. The F E E G consisted of frequencies up to 200 c/sec with
265
dominant rates between 40 and 120 c/sec. A distinctive large "spiking" wave form, typically triphasic, was regularly seen. Amplitude correlations between FEEG and SEEG would suggest that the EEG above 50 c/sec contains substantial elements of brain origin. REFERENCES ADRIAN, E. D. Discharge frequencies in the cerebral and cerebellar cortex. J. Physiol. (Lond.), 1935, 83:32 33. ~BAUMANN,m., BAUMANN,H. und BIELECKE,F. Neuronale Entladungsmuster schnellster elektrobiologischer Aktivit~iten und impulsf6rmiger Signale im Neo-, Allound Subkortex. Acta biol. reed. german., 1964, 12: 394-420. DROHOC~I, Z. ~lectrospectographie qualitative et quantitative du cerveau. Arch. Swiss Neurol. Psychiat., 1945, 55: 85-128. GOLDRING,S. and O'LEARY, J. L. Experimentally derived correlates between ECG and steady cortical potentials. J. Neurophysiol., 1951, 14: 275-288. GOZZANO, M. Ricerche sui fenomeni elettrici della corteccia cerebrale. Riv. Neurol., 1935, 8: 212-261. IL'tANOK, V. A. [A method for studying high frequency potentials of the electroencephalogram.] Biofizika, 1960, 5:488-492 (in Russian). KAISER, E. and PrTERS~N, I. Frequency analysis of muscle action potentials during tetanic contraction. Electromyography, 1963, 3: 5-17. LION, K. S., WINTER,D. F. and LEVIN, E. Electrical activity of the brain measured in the frequency range above 200 cycles per second. Electroenceph. clin. Neurophysiol., 1950, 2: 205-208. MARK, D. D. Electromyographic interference in the human electroencephalogram. Amer. J. Physiol., 1947, 149: 538-548. SCHLAG, J. and ]]ALVIN, R. Background activity in the cerebral cortex and reticular formation in relation with electroencephalogram. Exp. NeuroL, 1963, 8: 203-219. SCHWARTZ,M. Information transmission, modulation, and noise. McGraw-Hill, New York, 1959, 170 p. SCHWARZER, F. Ein Elektroencephalograph mit hohen Frequenzeigenschaften und geraden Koordinaten, mit einigen Bemerkungen zur Eiurichtung von EEGApparaten, Arch. Psychiat. Nervenkr. u. Z. Neurol., 1949, 183: 257-275. TRABKA, J. High frequency components in brain wave activity. Electroenceph. clin. Neurophysiol., 1962, 14: 453-464.
Reference: HALL,R. A., YEAGER,C. and YARBROUGH,R. B. Observations on high frequency electroencephalograms. Electroenceph. clin. Neurophysiol., 1967, 22: 262-265.
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
CLINICAL
AND
LABORATORY
NOTES
DIAGNOSTIC RECORDING OF SOMATO-SENSORY CORTICAL EVOKED POTENTIALS IN M A N L. BERGAMINI, B. BERGAMASCO, L. FRA, G . GANDIGLIO AND R . MUTANI
Neurological Clinic, University of Turin, Turin (Italy) (Accepted for publication: September 7, 1966)
The study in man by integration techniques of the response elicited in the specific cortical area by contralateral somaesthetic stimulation (electrical stimulation of a nerve) may be of considerable clinical importance. Significant data for diagnostic purposes have already been recorded by this technique in peripheral and spinal nerve lesions (Alajouanine et al. 1958; Halliday and Wakefield 1963; Giblin 1964; Bergamini et al. 1965, 1967). This report deals with an unusual diagnostic application of this neurophysiological technique in a pair of female Siamese twins who were studied before successful surgical division. CASE The two dorsally-linked, 6-year-old, Siamese female twins presented a very rare abnormality (incidence of about one in 300,000 newborns). The junction involved the gluteal soft parts, the sacrum and coccyx, with fusion of rectal and urogenital terminal parts (anus and vagina in common). They had been followed in the Pediatric Clinic of Turin University from their birth until their separation: complete details have been described by Gomirato-Sandrucci et aL (1966). A neurophysiological investigation was requested before surgery to determine, if possible, the absolute independence of their peripheral nervous pathways, since they had a vertebral segment in common. The idea of a possible common sacral or lumbosacral peripheral nervous pathway was supported: (1) by the fusion of the sacral spinal colurfffi; (2) by the presence of marked atrophy of the medial surface of the thigh muscles of the "internal" limbs, which is dorsally visible (Fig. 1) in the right lower limb in the left twin and in the left lower limb in the right twin; (3) by the dubious results of clinical examination of the general sensitivity and of the reflexes. In fact, due to the psychological condition provoked by years of Siamese life, surface sensory stimuli and proprioceptive tapping on the leg of one twin sometimes seemed to produce a remarkable response in the other twin. On the contrary, favouring independent nervous systems of the sisters was the consideration that the vertebral
fusion was too low to involve nerve roots immediately at their exits from the intervertebral foramina. At the surgeon's request for a detailed neurophysiological investigation to clarify any doubts concerning the presence of common peripheral nerve fibres, we decided to utilize the somato-sensory cortical evoked potential. If there were even minimal common lumbo-sacral peripheral nerves, stimulating a nerve in one twin's lower limb should produce an evoked response in the somaesthetic cortical area of the other twin. METHOD The lateral popliteal nerves at the heads of the fibulae of the twins' four lower limbs were stimulated by supramaximal electrical shocks with a 0.5/sec frequency, delivered from a constant current stimulator through surface electrodes. Recordings (4 channels) were made simultaneously of the activity evoked from the contralateral and ipsilateral somaesthetic areas with regard to the stimulated limb, and from both somaesthetic cortical areas of the other twin. The electrodes were placed on the cranial projection of the "leg" cortical area according to Kr6nlein (1898). The evoked somato-sensory responses were recorded with bipolar connections from the scalp and were averaged by means of a CAT 400 B (Mnemotron Corp.). The E E G was always simultaneously recorded. Two to three hundred cortical responses were averaged in order to detect even the smallest evoked potential. H reflex investigation with an E M G apparatus was also performed in all four limbs. This consisted in submaximal stimulation of the posterior tibial nerve in the popliteal fossa of one limb and detection of the motor reflex response in the sural triceps of each of the four limbs. RESULTS The response evoked in the post-Rolandic area to somaesthetic stimulation of a contralateral lower limb of each subject was always individual and physiological (Fig. 1). In other words, no activity recorded from the subject's scalp was ever found in the twin whose lateral popliteal nerve was not simultaneously stimulated on the opposite side.
Electroenceph. clin. Neurophysiol., 1967, 22:260-262
26l
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la colonne lombo-sacr6e, l'enregistrement du potentiel cortical 6voqu6 somesth6sique a 6t6 eraploy6 pour d6terminer la complete ind6pendance des fibres nerveuses spinales sensitives. La stimulation du nerf sciatique poplit6 exter•e d'une jumelle n'a jamais donn6e une r6ponse corticale enregistrable sur le cuir chevelu de l'autre jumelle. En outre, le r6flexe H n'a jamais 6t6 obtenu en dehors du membre inf6rieur stimul6. L'intervention chirurgicale a confirm6 la complete ind6pendance des syst~mes nerveux p6riph6riques des jumelles.
REFERENCES BARBIZET, J., CALVET, J. et VERLEY,R. Potentiels 6voqu6s corticaux chez des sujets atteints de troubles somesth6siques. Rev. neurol., 1958, 98: 757-761. BERGAMINI, L., BERGAMASCO, l . , FRA, L., GANDIGLIO, G., MOMBELLI,A. M. and MUTANI, R. Somato-sensory evoked cortical potentials in subjects with peripheral nervous lesions. Electromyography, 1965, 5: 121-130. BERGAMINI, L., BERGAMASCO, B., FRA, L., GANDIGLIO, G., MOMBELLI, A. M. et MUTANI, R. R6ponses corticales et p6riph6riques 6voqu6es par stimulation du ALAJOUANINE, T . , SCHERRER, J.,
Electroenceph. clin. Neurophysiol., 1967, 22:260-262
L. BERGAMINI et al.
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nerf dans la pathologie des cordons post6rieurs. Rev. neurol., 1967, in press. GIBLIN,D. R. Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann. N. Y. Acad. Sci., 1964, 112: 93-141. GOMIRATO-SANDRUCCI,M., MUSSA, G. C. e MARCHESE, G. S. I gemelli siamesi (illustrazione di una coppia di gemelle pigopaghe). Minerva pediat., 1966, 18:11211150.
HALLIDAY,A. M. and WAKEFIELD, G. S. Cerebral evoked potentials in patients with dissociated sensory loss. J. NeuroL Neurosurg. Psychiat., 1963, 26: 211-219. KR()NLEIN, R. U. Ztlr cranio-cerebralen Topographie. Beitr. klin. Chirurg., 1898, 22: 364-370. SOLERIO, L. Separazione di due gemelle congiunte pigopaghe (nota preventiva). Minert,a reed., 1965, 56: 1-4.
Reference: BERGAMINI,L., BERGAMASCO,B., FRA, L., GANDIGLIO,G. and MUTANI,R. Diagnostic recording of somatosensory cortical evoked potentials in man. Electroenceph. clin. Neurophysiol., 1967, 22: 260-262.
OBSERVATIONS
ON HIGH FREQUENCY
ELECTROENCEPHALOGRAMS 1 R . A . HALL, M . D . , C. YEAGER, M . D . AND R . B. YARBROUGH, P H . D .
Psychophysiological Research Laboratory, Institute for Medical Research of Santa Clara County, San Jose, Calif. (U.S.A.) (Accepted for publication: August 31, 1966) INTRODUCTION From the point of view of information theory, to obtain all the information contained in a signal, all frequency components present must be examined (Schwartz 1959). Therefore, to obtain additional information about the brain from its transmitted electrical potentials, all frequency components should be studied. This report considers activity up to 250 c/sec. It would appear that technical rather than theoretical reasons have, in the past, limited study of the E E G signal to frequency components from about 1 to 50 c/sec. The lower limit appears to have been set by problems of electrode polarization and the instability of early D C amplifiers. Recent work by Goldring and O'Leary (1951) on steady potentials has shown that valuable information is obtainable from the EEG signal by extending the lower frequency limit. Study of higher frequencies seems to have been restricted by the physical capabilities of the inkwriting oscillograph. Mostly using cathode ray oscillography, a number of workers have looked at the higher frequencies beginning with Gozzano (1935). Adrian (1935) reported frequencies above 200 c/sec from the cerebellum. According to Drohocki (1945), the existence of frequencies up to 200 c/sec of cerebral (and non-muscular) origin is incontestable. Recording from the h u m a n scalp and exposed cat cortex, Lion et al. (1950) found potentials up to 70/~V in the 200-1400 c/sec range. Recording a rectified presentation 1 This work was supported, in part, by a grant from the Scottish Rite Committee for Research in Schizophrenia.
of components in the 100-13,000 c/sec range from implanted depth electrodes in the cat brain, Schlag and Balvin (1963) reported that this "background activity" varies with probe location and shows high correlation with and often prediction of changes in standard EEG. Baumann et al. (1964) reported activity up to 5800 c/sec using depth probes in animal brains. Schwarzer (1949) described an E E G machine employing a stylus and carbon-paper method which produces records having a fiat response up to 200 c/sec. However, we have found no reports of the application of this machine to study of high frequency EEG. The same applies to II'ianok's (.1960) modification of the Grey Walter harmonic analyzer which extends its range to 480 c/sec. The present report describes a method of obtaining paper records of "fast E E G " (FEEG) free of the lower frequencies which characterize the "'standard E E G " (SEEG). Sample records are presented along with findings from the study of many such traces. METHOD Beckman electrodes 2 were applied at Fp~, C3 and O1, according to the International 10-20 System. The signal source of channel I was Fp~ and C3 and for channel It was C3 and O1. A negative potential on Cz produces a downward pen-deflection in channel I and an upward deflection in channel II. The specially built Cemco amplifiers 3 have an input impedance of 200 kf2 and selectable band passes of 50-250 c/sec or 1-50 c/sec with 12 db per octave roll-off produced by active filters. Maximum peak 2 Beckman Instruments Co., Palo Alto, Calif. California Electronics Manufacturing Co., Alamo, Calif.
Electroenceph. olin. Neurophysiol., 1967, 22:262-265
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; IOOms~ Fig. 1 S a m p l e t r a c e s o f F E E G a n d B E E G . A l l E E G t r a c e s are F E E G e x c e p t B E E G i n first a n d s e c o n d t r a c e s o f ( A ) a n d third a n d f o u r t h t r a c e s in ( F ) . T i m e c a l i b r a t i o n o f 100 m s e c at t o p a n d b o t t o m a p p l y to all t r a c e s e x c e p t t h o s e in (C). T r a c e s (A) t h r o u g h ( E ) are f r o m a 4 2 - y e a r - o l d f e m a l e : (A) basal state traces, (B) b a s a l state F E E G 1 m i n later, ( C ) C R O p h o t o g r a p h s o f w h i c h left is 10 k c n o i s e , o t h e r s are F E E G at a b o u t s a m e t i m e as ( B ) , ( D ) t r a c e s o n a n o t h e r day, a n d ( E ) t r a c e s w h i l e r e a d i n g . T r a c e s m ( F ) are f r o m a 3 8 - y e a r - o l d f e m a l e u n d e r lateral eye m o t i o n , first left a n d t h e n right, o n v o i c e c o m m a n d s r e c o r d e d in b o t t o m trace.
R . A . HALL et al.
264
to peak noise in the higher band pass is 2 # V with shorted input and 4.8/zV with a 10 kf~ input resistor. To show the simultaneous relationship between F E E G and SEEG, the unfiltered Cemco pre-amplifier output was led (in 4 cases) into Tektronix 122 pre-amplifiers set at a band pass of 0.2-250 c/sec, yielding " b r o a d band E E G " (BEEG). All signals were recorded on magnetic tape with a Precision Instruments Co. Model PS 207A F M systemL Paper records were made off-line on a Model 6 Grass E E G machine 2, with taped signal played at half speed. This yielded oscillographic records of the F E E G with the 3 db frequency point thus raised from the usual 70 c/sec to 140 c/sec and with attenuation of the frequencies below 50 c/sec (about --30 db for the alpha activity). Recordings were made in a moderately illuminated and grounded Faraday Cage. Subjects were fourteen normal persons, half of each sex, ranging from 26 to 61 years of age. None had a history of epilepsy, of abnormal EEG, or of taking any medication for at least 7 da}s, aside from aspirin and insulin (by one diabetic woman). All were right-handed. A recording in a relaxed basal state with eyes closed (BS) was takenfrom thirteen subjects. The usual procedure was to first record the F E E G for 10 min and then the SEEG for 5 min. However, in four cases B E E G and F E E G were recorded simultaneously for 10 min, In ten subjects a 5 min sample with eyes open was also taken, always prior to the basal state record, and in one subject this constituted the entire record. Records were obtained from three subjects performing lateral and vertical eye movements on voice command which was recorded simultaneously with B E E G and FEEG. A record was taken from one subject while reading in order to show the effects of muscular artifacts. The results reported here are derived from visual study of the entire ink-written records. All parameters were quantified as far as possible. All SEEGs and BEEGs were interpreted to be normal in regard to the lower frequency patterns. Maximum amplitude was taken as the largest peak to peak voltage. Average amplitude was estimated by scanning the entire record to obtain a mean level. Frequency estimations were made by a combination of counting waves per unit time and measuring periods. Statistical measures were based on the assumption of a normal population. The student t statistic was used in all cases.
RESULTS
General The F E E G records varied considerably from subject to subject, whereas for any given subject the Fpl-C8 and C8-O1 wave patterns appeared to be similar. With simultaneous recording of F E E G and B E E G no consistent relationship was observed between particular F E E G waves (such as the "spikes" to be described below) and the slow waves. Precision Instruments Co., Palo Alto, Calif. 2 Grass Instrument Co., Quincy, Mass.
Sample records In Fig. 1, A the F E E G records show typical high frequency activity. The mean amplitudes in Fpl-Ca and C~-O1 are 10 and 6/zV respectively (noise level: 3/~V). The frequency range, excluding "spikes", is from 50 to 120 c/sec. The peak amplitude of about 2 5 / t V is contributed by "spikes" occurring at a rate of about 20/sec. These are predominantly synchronous in the two derivations with opposing polarities. While the "spiking" appears in both F E E G and BEEG records, there is no obvious correlation between the alpha wave form and the FEEG. In B, the "spiking" activity is similar but of smaller amplitude. (See legend for further explanations.) The record E (taken while this subject was reading) shows the difference between bursts of large amplitude muscular artifacts and the ongoing F E E G in Fpl-Ca; the smaller amplitude portion contains activity similar to that of the basal state, while the muscular activity is characterized by periods of 3-10 msec per phase. The Ca-O~ derivation remains unaffected by the muscle contraction, but still shows ongoing high frequency waves. The records in F are from another subject performing lateral eye movements. In both the F E E G and B E E G traces of Fp~-Ca triphasic waves with phase periods of 7-18 msec are observed, apparently initiating the slower transient in the BEEG trace.
Measurements I. Amplitude. Measurements were made of F E E G records (obtained during the eyes open condition) for both Fpl-C3 and C~-O1, in ten subjects for a total of 20 measurements each of average and maximum voltage. Similar measurements of BS F E E G records were made in thirteen subjects for a total of 26 measurements each of average and maximum voltages. The mean of the 46 average measurements was 8.3/~V (range 4-20 #V) and the mean of the maximum measurements was 23.4/~V (range 7-90/~V). The 23 FpI-C8 traces showed a mean for average voltage measurements of 9.6/~V as compared to 7.0 #V for the 23 C8-O1 traces, a difference that is not statistically significant ( P : 0.1). The mean of 14 BS measurements of average F E E G voltage in seven females was 10.6/~V as compared to 6.0 pV for 12 measurements insix males, a difference significant at the 2 % level. Examination of both average and maximum measurements of the anterior F E E G failed to demonstrate any significant difference between the eyes open and basal state. Positive correlations ( P = 0.05) were found between the F p l - C s basal state SEEG (or BEEG) maximum amplitude and both the maximum F E E G amplitudes (in both conditions) in FpI-C3 and C3-O1. Significant (P = 0.05) correlations were found between all F E E G maximum amplitudes, and between all F E E G average amplitudes except for the correlation between eyes open in Fpl-Ca and basal state in C8-O1. II. Frequency. Frequencies ranging up to 200 c/sec were observable in the records, sometimes in runs of about 5 waves of up to 10/zV amplitude at the upper frequency
Electroenceph. clin. Neurophysiol., 1967, 22:262-265
HIGH FREQUENCY EEG limit. Dominant rhythmicities of 80-100 c/sec were often seen. The mean of highest observable frequencies in 23 anterior traces was 139 c/sec and for 22 posterior traces was 120 c/sec, a difference which is not significant (P = 0.2). Ill. Morphology. The "spiking", triphasic waves of about 30 msec total duration, were the only obvious wave form characteristic of the F E E G and were regularly observed in all records. They tended to be synchronous in Fpl-C3 and C3-O1, with opposite or same polarity. Their rate of occurrence would range from 7 to 20/sec, occasionally reaching 40/sec. DISCUSSION The records of muscle artifact and directed eye movement showed periods similar to the F E E G "spiking". Considering this and the fact that the frequency range of the F E E G and that of muscular contractions (see Kaiser and Peters6n 1963) overlap, the question of E M G origin of much of the F E E G must be raised. This is particularly true for anterior derivations where muscle potentials are commonly present in the standard EEG (see Mark 1947). The trend toward higher potentials in Fpl-C3 is consistent with this possibility. However, the F E E G during eyes open, in which we might expect more muscular potentials anteriorly, showed no significant difference from the F E E G of the basal state. A common brain signal source is suggested by the amplitude correlations between the basal anterior SEEG and the FEEG. The "spiking" potentials strikingly resemble Trabka's (1962) examples of sensory evoked high frequency potentials in the cortex of the Nembutalized cat, suggesting brain origin of at least this component of the FEEG. Regularly obtaining these "spiking" F E E G records from normal subjects suggests that they may be a normal neurophysiological phenomenon. SUMMARY EEG potentials from the dominant hemisphere of fourteen normal persons were recorded on magnetic tape with high (50-250 c/see) and low (1-50 c/sec) or broad (0.2-250 c/see) band pass filtering. Write-out was obtained from a standard EEG machine with the taped signal played at half speed. This yielded an oscillographic record of the filtered "fast E E G " (FEEG) freed of effects of the lower frequencies. In the eyes-closed resting state FEEG-, the group mean of average amplitude was 8.3 ~V and the mean of maximum amplitudes was 23.4 #V. The amplitudes showed a correlation between F E E G and standard EEG. The F E E G consisted of frequencies up to 200 c/sec with
265
dominant rates between 40 and 120 c/sec. A distinctive large "spiking" wave form, typically triphasic, was regularly seen. Amplitude correlations between FEEG and SEEG would suggest that the EEG above 50 c/sec contains substantial elements of brain origin. REFERENCES ADRIAN, E. D. Discharge frequencies in the cerebral and cerebellar cortex. J. Physiol. (Lond.), 1935, 83:32 33. ~BAUMANN,m., BAUMANN,H. und BIELECKE,F. Neuronale Entladungsmuster schnellster elektrobiologischer Aktivit~iten und impulsf6rmiger Signale im Neo-, Allound Subkortex. Acta biol. reed. german., 1964, 12: 394-420. DROHOC~I, Z. ~lectrospectographie qualitative et quantitative du cerveau. Arch. Swiss Neurol. Psychiat., 1945, 55: 85-128. GOLDRING,S. and O'LEARY, J. L. Experimentally derived correlates between ECG and steady cortical potentials. J. Neurophysiol., 1951, 14: 275-288. GOZZANO, M. Ricerche sui fenomeni elettrici della corteccia cerebrale. Riv. Neurol., 1935, 8: 212-261. IL'tANOK, V. A. [A method for studying high frequency potentials of the electroencephalogram.] Biofizika, 1960, 5:488-492 (in Russian). KAISER, E. and PrTERS~N, I. Frequency analysis of muscle action potentials during tetanic contraction. Electromyography, 1963, 3: 5-17. LION, K. S., WINTER,D. F. and LEVIN, E. Electrical activity of the brain measured in the frequency range above 200 cycles per second. Electroenceph. clin. Neurophysiol., 1950, 2: 205-208. MARK, D. D. Electromyographic interference in the human electroencephalogram. Amer. J. Physiol., 1947, 149: 538-548. SCHLAG, J. and ]]ALVIN, R. Background activity in the cerebral cortex and reticular formation in relation with electroencephalogram. Exp. NeuroL, 1963, 8: 203-219. SCHWARTZ,M. Information transmission, modulation, and noise. McGraw-Hill, New York, 1959, 170 p. SCHWARZER, F. Ein Elektroencephalograph mit hohen Frequenzeigenschaften und geraden Koordinaten, mit einigen Bemerkungen zur Eiurichtung von EEGApparaten, Arch. Psychiat. Nervenkr. u. Z. Neurol., 1949, 183: 257-275. TRABKA, J. High frequency components in brain wave activity. Electroenceph. clin. Neurophysiol., 1962, 14: 453-464.
Reference: HALL,R. A., YEAGER,C. and YARBROUGH,R. B. Observations on high frequency electroencephalograms. Electroenceph. clin. Neurophysiol., 1967, 22: 262-265.