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Depth electrographic observations in two cases of photo-oculoclonic response
ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYS[OLOGY
71
DEPTH ELECTROGRAPHIC OBSERVATIONS IN TWO CASES OF PHOTO-OCULOCLONIC RESPONSEI.~ G. E. CEIATRIANa A N D C. PEREZ-BORJA4
EEO Laboratory, Rochester State Hospital, Rochester, Minn. (U.S.A.) (Accepted for publication: October 15, 1963) Gastaut (I 950a) as"fronto-polar response by recruitment" and later renamed by Bickford et al. (1952) "photomyoclonic response". The present study provides pertinent information derived from concomitant surface and depth electrograms and correlates it with previous findings.
INTRODUCTION
The physiological mechanisms underlying the oculoclonic response to intermittent photic stimulation are still controversial, This phenomenon was first described by
Photic S tim...~,, .;
•
~
-
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'
L
II
' '
..
'
,lIJ
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~
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.. 2"...
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Fig. I Typical photo-oculoclonic response recorded in conventional surface electrograms on a 40 year old woman suffering from psychotic depression. ,b
1 This study was pattiaiiy supported by a grant from the Minnesota Department of Public Welfare to the Rochester State Hospital. s Read, in part, at the Round Table Discussion on Depth Recordings from the Human Brain, Fifth International Congress of Electroencephalography and Clinical Neurophysiology, Rome, September 7-13, 1961. a Present address: EEG Laboratory, University Hospital, University of Washington School of Medicine, Seattle, Washington. 4 Present address: Division of Neurology, Wayne State University College of Medicine, Harper Hospital, Detroit, Michigan.
MATERIAL AND METHOD
Observations were made on two patients, a 40 year old woman suffering from psychotic depression with no history of epilepsy, and a 36 year old woman with chronic intractable temporal lobe seizures not precipitated by photic stimuli. Multi.~lectrode leads were implanted into various areas of the brain of these patients through burr-holes intended for later lee in frontal lobotomy in one case and in temporal Iobectomy in the other. Each lead consisted of seven strands of stainless steel wire insulated with formvar except at the tips (Chatrian et aL 1959). Deep and superficial electrograms were obtained with Electroeneeph. clin. Neurophysiol., 1964, 17:71-75
72
G. E. CHATRIAN AND C. PEREZollORJA
a 16-chennel ©lectroenccphalompraph(Grass) and a 4-heam cathode-ray osciUolpraph (Electronic Tube Corporation). A stroboscope (Grass Model PSI) was used as an intermittent light source.
RESULTS Both patients exhibited a typical oculoclonic response with photic stimulation at 10-20 flashes/see in pre-operarive scalp e l e c t ~ (Fig. I). The response consisted of a succession of brief 'spikes" and slow waves which increased gradually in amplitude during the first few seconds of stimulation, then waxed and waned, abruptly subsiding with cessation of stimulus. Rhythmical contractions of the peri.orbital muscles and vertical oscillations of the eyeballs appeared to be intimately related to the response pattern.
R
Following implantation of depth electrodes the same response was elicited while recording simultaneously from the surface of the scalp and the depth of the brain (Fig. 2). The recordings from wit~n the brain tissue exhibited a C~'iving response which had the same frequency or a frequency harmonically related to that of the flashes. In both subjects, the responseirradiated widely from the posterior to the most anterior areas of the brain. In the frontal lobe, the response increased in voltage at the onset of stimulation and then waxed and waned (Fig. 2). Its voltage was at times greater than that of the occipital response. Whereas potentials derived from the peri-orbital muscles and those due to the rotation of the eyeballs around their transverse axis appeared to contribute greatly to the re, sponserecorded by surface electrodes,suchpotentials were extraneous to the response picked up from within the
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......
Fig, 2 Surface and depth electrograms recorded during photo-oculoclonic response on the same patient as in Fill. I.
Electroenceph. clin. IYeurophysiol., 1964, 17: 71-?$
PHOTO.OCULOCLONIC RESPONSE frontal and temporal lobes. In fact, voluntary contractions of the facial musculature and repeated voluntary or random spontaneous eyeblinks failed to provoke any recordable signal in depth electrograms (Fig, 2), The patient suffering from temporal lobe seizures manifested oculoolonus and concomitant frontal irradiated response also with paired flashes separated by an interval of 50 msec delivered randomly or repeated at a rate of !-5 flash-pairs/see. With this technique (Gastaut and Corriol 1951), a response was recorded by surface peri-~rbital electrodes (Fig. 3 and 4) which consisted of a R
73
more. The mean latency of the responses recorded bipolarly between electrodes located in the anterior portion of the parietal lobe was 65 msec (from the second flash to the first spike). The latencies were 3-5 msec shorter in the posterior portion of the temporal lobe and 7-10 rnsec longer in the frontal lobe (Fig. 5). The voltage of the responses measured as much as 150 pV from peak to peak in the frontal lobe. DISCUSSION The history of investigations on the mechanisms of
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2 6
Fig. 3 Photo-oculoclonus provoked by stimulation with I/see flash.pairs separated by a 50 msec interval. Simultaneous recording from surface peri.orbital aod from depth electrodes on a 36 year old woman with chronic intractable temporal lobe seizures. brief spike of low voltage followed by a slower diphnsic wave of higher potential. Simultaneous EEG recordin8 from within the substance of the frontal lobe and of more posterior areas of the brain showed complex responses represented by multiple brief spikes and slower waves, Oscilloscopic tracings (Fig. 5) revealed that they usually consisted of a brief triphasic spike followed by a slower diphasie deflection, Their total duration was 150 msec or
the photo-oculocloni¢ response is complex. Oastaut (1950a) characterized the response by the occurrence of "frontal polyspikes" increasinggradually in amplitude as in a recruiting response. He emphasized the interest of the "production under the influences of Metrazol or of certain diencephalic disorders and with well chosen frequencies of stimulation, of electrical paroxysms appearing in regions very distant from the occipital lobes and particularly in
Electroenceph. clin. Neurophysiol., 1964, 17:71-75
74
G. E. CHATglAN AND C. PEREZ-BORJA
|
,4 ;
..... ei
b*
I
A
B
Fig, 4 Surface peri-orbitaland depth recordings of photo-oculoclonic response with I/see (Section A) and 31see (Section B) flash-pairsseparated by a .~0 ms~ interval, The patient is the same as in Fig, 3.
Fill, 5 Os¢illollraphic recordlngs of the responses to double flash stimulation from electrodes I 1-12 and 40-39 who~e approximate locatioa is depicted in Fig 4 (Time marker: 40 c/see) The patient is the same as in Fill. 3. the frontal lobes". Later, Gastaut (1950b) referred to this response as one "ip which the neuronal discharge following a flash of light does not remain strictly localized to the optic regions but spreads to the whole cortex and even paradoxicall/, predominates in the frontal regions". The concomitant muscular response presented "the same recruiting features as the cortical response" Experimental studies by Gastaut and Hunter (1950) and by Gastaut et al (1951) of the ~rradiation phenomenon with photi¢ stimulation combined with Metrazol injection appeared to support these finditt~ However, Gastaut's interpretation of the fronto-polar response was challen~'d by Bickford and Daly (1951) who emphasized the "contribution of extracranial potentials ~aerated by scalp muscles and eye movement to the myoclonic response". Gastaut then acknowledged the difficulty cf "ascertaining definitely the muscular or cor_ical origin of this response" (1951) and finally conceded: "I make a
distinction essentially betwecn the fronto.polar response (that 1 have called elsewhere "by recruitment") which i have no doubt is of palpebml origin, and the frontorolandic response which is, on the contrary, of essentially cortical origin" (1952). Further evidence in favor of the muscular origin of the response was presented by Bickford et al. (1952) who suggested that this phenomenon "may be regarded as a normal response mechanism to high. intensity repetitive illumination in the human being. Its oo:arrence would seem to have little clinical significance except in ~re instances in which the response is pathologically exaggerated (some varieties of myoclonic epilepsy)". The term "photo.myoclonic" response was proposed by these authors to stress the purely muscular nature of this phenomenon and to differentiate it from the "photoconvulsive response" (fronto-rolandic response of Gas. taut) which is observed essentially in epileptic subjects and can be induced in normal subjects by injection of MetraElectroenceph. clin. Neurophysiol., 1964, 17:71-75
75
PHO'fO-OCULOCLONIC RESPONSE zol. T h e e interpretations, agreed upon by the partici. pants in a panel discussion on Photo.Metrazol Activation of the EEG (1952), were later re-emphasized by Bickford et al. (1953). Johnson and Bickford (1953) also challenged experimentally the earlier findings of Gastaut and Hunter (1950). The present study of simultaneous recordings from the surface of the scalp and from within the brain, suggests that in two patients investigated the photo-oculoclonic response consisted of several recordable components. The response recorded by surface electrodes appears to contain brief spikes arising from the peri-orbital musculature and slower oscillations produced by the rhythmic displacement of the cornco-retinal potential in the course of ocoloclonus. In response to paired flashes the initial brief spike is probably muscular in origin, whereas the following slow diphasic wave is presumably due to the rotation of the eyeball around its transverse horizontal axis (R~mond 1952). in surface electrograms the cortical component of the response is largely masked by these muscular and ocular components but it is clearly evident in recordings with intracerebral electrodes. The mechanism of the cerebral response irradiating to the frontal lobes deserves further study. The increase in latency of the irradiation potentials with increasing dis. tahoe from the o~ipital areas suggests that transeortieal irradiation from the visual cortex has a dominant role in this phenomenon. This conjecture is in agreement with the experimental data of Hunter and lngvar (1955) on the irradiated responses to photic stimulation combined with subconvulsive doses of Metrazol. Whether the present results can be applied to all oculoeloni¢ responses with photic stimulation must still be determined. However, it appears that from the demonstration in conventional scalp recordings of the electro. myographi¢ and electro-oculographic concomitants of oculoclonus the absence of a simultaneous frontal irradiation of cortical evoked g~tentials cannot be inferred. SUMMARY Simultaneous deep and supefikial electrograms recorded in two patients with typical "photo.o~ulocloni¢ response" ("fronto.polar recruiting response" of Gastaut or "photo.myoclonic response" of Bickford) suggest that the response consisted in these cases of several recordable components. Surface recordings contained potentials es. sentially muscular and ocular in origin whereas depth electrograms revealed long latency frontal irradiation potentials. No definite clinical diagnostic significance is attributed to the phenomenon of frontal irradiation of visual responses in the human.
REFERENCES BiCI~ORD, R. C. and DALY, D. Experiences with photometrazol test. Electroenceph. clin. Neuropbysiol., 1951, 3: 378. BICKrOP.D,R. G., SEM-JAcoBsEN,G. W., Wsrre, P. T. and D^LY, D. Some observations on the mechanism of photic and Photo-Metrazol activation. Electroenceph. clin. Neurophysiol., 1952, 4: 275-282. BICKFORD,R. G., WHITE,P. T., SEM-JAcoasEN,C. W. and RODIN, E. A. Components of the photomyoclonic response in man. Fed. Prec., 1953, 12: 15-16. CHATRIAN, G. E., POLLACK,C. S. and PETEasEN, M. C. A procedure for preparing a multielectrode lead for intracerebral recordings. F.lectroenceph. clin. Neuro. physiol., 1959, 11: 358-361. G~TAtrr, H. Combined photic and Metrazol activation of the brain. Electroenceph. cli.,~. Ne~7,hvsiol., 1950a, 2: 249--261. G~TAtn, H. Un signe 61ectroenc~phalographique des hydroc~phalies: la r6ponse par recrutement au cours de la stimulation lumineuse intermittente. Rev. neurol., 19g0b, 82: 410-413. GASTAUT,H. Lea deux types de r6ponses photiques irra. di6es chez I'homme. La d~barge myoclonique hyper. syn0hrone et la d~charge myoclonique par recrute. ment. Riv. Neurol., 1951, 21: 27-37. GAST^UT,H. L'activation photo-eardiazolique. Electroen. eeph. ella. Neurophysiol., 1952, 4: 271-274. GASTAUT, H. et COt~RmL, J. Note pr~liminaire sur un proc~16 nouveau et particuli6rement eliicace de stimulation lumineuse intermittente. Eleetroenceph. din. Neurophyslol., 19aJI, 3: 87-88. GASTAUT,H. and HUN~R, J. An experimental study of the mechanism of photi¢ activation in idiopathic
epilep#y. £1ectroeneepk. eBn. Neuropkyslol., ~19'30,2: 263-287. GASTAUT,H,, NAQUL'T,R. et Rooee, A. Cycle d'excitabi. lit6 du cortex frontal au cours de la r6ponse irradi~e photique chez le chat. C.R. Soc. Biol. (Palb), 1951, 145: 1339-1340. H U N ~ , J. and INOVAtX, D. H, Pathways mediating metrazol induced irradiation of visual impulses. £1ee. troenceph, din. Neurophysiol., l~J& 7: 39-60. JOHNSON, D. A. and BICKeOt~D,g. G. Factors affecting cortical, subcortical and myoclonic responses to photic stimulation in cats. £1ectroeneeph. din. NeurophysioL, 1953, 5: 126. RI[MOND, A. In SYtOO#IUM, Photo.Metrazol activation of the EEG. Discussion. £1eetroeneeph. elin. NeurophysloL, 1952, 4: 303--310. SYMPOSIUM.Photo-Metraxol activation of the EEG. Dis-" cussion. £1eetroenceph. din. Neurophy.ffol., 1952, 4: 303-310.
Reference: CHATRIAN,O. E. and PEREZ-BOP.JA,C. Depth electrographic observations in two cases of photo-oculoclonie response. Eleetroenceph. clin. Neurophyslol., 1964, 17: 71-75.
71
DEPTH ELECTROGRAPHIC OBSERVATIONS IN TWO CASES OF PHOTO-OCULOCLONIC RESPONSEI.~ G. E. CEIATRIANa A N D C. PEREZ-BORJA4
EEO Laboratory, Rochester State Hospital, Rochester, Minn. (U.S.A.) (Accepted for publication: October 15, 1963) Gastaut (I 950a) as"fronto-polar response by recruitment" and later renamed by Bickford et al. (1952) "photomyoclonic response". The present study provides pertinent information derived from concomitant surface and depth electrograms and correlates it with previous findings.
INTRODUCTION
The physiological mechanisms underlying the oculoclonic response to intermittent photic stimulation are still controversial, This phenomenon was first described by
Photic S tim...~,, .;
•
~
-
' ......
'
L
II
' '
..
'
,lIJ
'
~
' !
I
+
.. 2"...
~,k,~,~*,--.,-.Eyes
closed I Sl[¢
Fig. I Typical photo-oculoclonic response recorded in conventional surface electrograms on a 40 year old woman suffering from psychotic depression. ,b
1 This study was pattiaiiy supported by a grant from the Minnesota Department of Public Welfare to the Rochester State Hospital. s Read, in part, at the Round Table Discussion on Depth Recordings from the Human Brain, Fifth International Congress of Electroencephalography and Clinical Neurophysiology, Rome, September 7-13, 1961. a Present address: EEG Laboratory, University Hospital, University of Washington School of Medicine, Seattle, Washington. 4 Present address: Division of Neurology, Wayne State University College of Medicine, Harper Hospital, Detroit, Michigan.
MATERIAL AND METHOD
Observations were made on two patients, a 40 year old woman suffering from psychotic depression with no history of epilepsy, and a 36 year old woman with chronic intractable temporal lobe seizures not precipitated by photic stimuli. Multi.~lectrode leads were implanted into various areas of the brain of these patients through burr-holes intended for later lee in frontal lobotomy in one case and in temporal Iobectomy in the other. Each lead consisted of seven strands of stainless steel wire insulated with formvar except at the tips (Chatrian et aL 1959). Deep and superficial electrograms were obtained with Electroeneeph. clin. Neurophysiol., 1964, 17:71-75
72
G. E. CHATRIAN AND C. PEREZollORJA
a 16-chennel ©lectroenccphalompraph(Grass) and a 4-heam cathode-ray osciUolpraph (Electronic Tube Corporation). A stroboscope (Grass Model PSI) was used as an intermittent light source.
RESULTS Both patients exhibited a typical oculoclonic response with photic stimulation at 10-20 flashes/see in pre-operarive scalp e l e c t ~ (Fig. I). The response consisted of a succession of brief 'spikes" and slow waves which increased gradually in amplitude during the first few seconds of stimulation, then waxed and waned, abruptly subsiding with cessation of stimulus. Rhythmical contractions of the peri.orbital muscles and vertical oscillations of the eyeballs appeared to be intimately related to the response pattern.
R
Following implantation of depth electrodes the same response was elicited while recording simultaneously from the surface of the scalp and the depth of the brain (Fig. 2). The recordings from wit~n the brain tissue exhibited a C~'iving response which had the same frequency or a frequency harmonically related to that of the flashes. In both subjects, the responseirradiated widely from the posterior to the most anterior areas of the brain. In the frontal lobe, the response increased in voltage at the onset of stimulation and then waxed and waned (Fig. 2). Its voltage was at times greater than that of the occipital response. Whereas potentials derived from the peri-orbital muscles and those due to the rotation of the eyeballs around their transverse axis appeared to contribute greatly to the re, sponserecorded by surface electrodes,suchpotentials were extraneous to the response picked up from within the
L
o
5
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7
1
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w
F[0~gS.. ~:h,--- . . . .
••••i•••••••••••••••|•••••••••i••••••••|•••••|••••••••|•••i|•••••••|••••••••••••|•|••|••i•i••••••••|•|••••i|i
p
......
Fig, 2 Surface and depth electrograms recorded during photo-oculoclonic response on the same patient as in Fill. I.
Electroenceph. clin. IYeurophysiol., 1964, 17: 71-?$
PHOTO.OCULOCLONIC RESPONSE frontal and temporal lobes. In fact, voluntary contractions of the facial musculature and repeated voluntary or random spontaneous eyeblinks failed to provoke any recordable signal in depth electrograms (Fig, 2), The patient suffering from temporal lobe seizures manifested oculoolonus and concomitant frontal irradiated response also with paired flashes separated by an interval of 50 msec delivered randomly or repeated at a rate of !-5 flash-pairs/see. With this technique (Gastaut and Corriol 1951), a response was recorded by surface peri-~rbital electrodes (Fig. 3 and 4) which consisted of a R
73
more. The mean latency of the responses recorded bipolarly between electrodes located in the anterior portion of the parietal lobe was 65 msec (from the second flash to the first spike). The latencies were 3-5 msec shorter in the posterior portion of the temporal lobe and 7-10 rnsec longer in the frontal lobe (Fig. 5). The voltage of the responses measured as much as 150 pV from peak to peak in the frontal lobe. DISCUSSION The history of investigations on the mechanisms of
L
f
3
2 6
Fig. 3 Photo-oculoclonus provoked by stimulation with I/see flash.pairs separated by a 50 msec interval. Simultaneous recording from surface peri.orbital aod from depth electrodes on a 36 year old woman with chronic intractable temporal lobe seizures. brief spike of low voltage followed by a slower diphnsic wave of higher potential. Simultaneous EEG recordin8 from within the substance of the frontal lobe and of more posterior areas of the brain showed complex responses represented by multiple brief spikes and slower waves, Oscilloscopic tracings (Fig. 5) revealed that they usually consisted of a brief triphasic spike followed by a slower diphasie deflection, Their total duration was 150 msec or
the photo-oculocloni¢ response is complex. Oastaut (1950a) characterized the response by the occurrence of "frontal polyspikes" increasinggradually in amplitude as in a recruiting response. He emphasized the interest of the "production under the influences of Metrazol or of certain diencephalic disorders and with well chosen frequencies of stimulation, of electrical paroxysms appearing in regions very distant from the occipital lobes and particularly in
Electroenceph. clin. Neurophysiol., 1964, 17:71-75
74
G. E. CHATglAN AND C. PEREZ-BORJA
|
,4 ;
..... ei
b*
I
A
B
Fig, 4 Surface peri-orbitaland depth recordings of photo-oculoclonic response with I/see (Section A) and 31see (Section B) flash-pairsseparated by a .~0 ms~ interval, The patient is the same as in Fig, 3.
Fill, 5 Os¢illollraphic recordlngs of the responses to double flash stimulation from electrodes I 1-12 and 40-39 who~e approximate locatioa is depicted in Fig 4 (Time marker: 40 c/see) The patient is the same as in Fill. 3. the frontal lobes". Later, Gastaut (1950b) referred to this response as one "ip which the neuronal discharge following a flash of light does not remain strictly localized to the optic regions but spreads to the whole cortex and even paradoxicall/, predominates in the frontal regions". The concomitant muscular response presented "the same recruiting features as the cortical response" Experimental studies by Gastaut and Hunter (1950) and by Gastaut et al (1951) of the ~rradiation phenomenon with photi¢ stimulation combined with Metrazol injection appeared to support these finditt~ However, Gastaut's interpretation of the fronto-polar response was challen~'d by Bickford and Daly (1951) who emphasized the "contribution of extracranial potentials ~aerated by scalp muscles and eye movement to the myoclonic response". Gastaut then acknowledged the difficulty cf "ascertaining definitely the muscular or cor_ical origin of this response" (1951) and finally conceded: "I make a
distinction essentially betwecn the fronto.polar response (that 1 have called elsewhere "by recruitment") which i have no doubt is of palpebml origin, and the frontorolandic response which is, on the contrary, of essentially cortical origin" (1952). Further evidence in favor of the muscular origin of the response was presented by Bickford et al. (1952) who suggested that this phenomenon "may be regarded as a normal response mechanism to high. intensity repetitive illumination in the human being. Its oo:arrence would seem to have little clinical significance except in ~re instances in which the response is pathologically exaggerated (some varieties of myoclonic epilepsy)". The term "photo.myoclonic" response was proposed by these authors to stress the purely muscular nature of this phenomenon and to differentiate it from the "photoconvulsive response" (fronto-rolandic response of Gas. taut) which is observed essentially in epileptic subjects and can be induced in normal subjects by injection of MetraElectroenceph. clin. Neurophysiol., 1964, 17:71-75
75
PHO'fO-OCULOCLONIC RESPONSE zol. T h e e interpretations, agreed upon by the partici. pants in a panel discussion on Photo.Metrazol Activation of the EEG (1952), were later re-emphasized by Bickford et al. (1953). Johnson and Bickford (1953) also challenged experimentally the earlier findings of Gastaut and Hunter (1950). The present study of simultaneous recordings from the surface of the scalp and from within the brain, suggests that in two patients investigated the photo-oculoclonic response consisted of several recordable components. The response recorded by surface electrodes appears to contain brief spikes arising from the peri-orbital musculature and slower oscillations produced by the rhythmic displacement of the cornco-retinal potential in the course of ocoloclonus. In response to paired flashes the initial brief spike is probably muscular in origin, whereas the following slow diphasic wave is presumably due to the rotation of the eyeball around its transverse horizontal axis (R~mond 1952). in surface electrograms the cortical component of the response is largely masked by these muscular and ocular components but it is clearly evident in recordings with intracerebral electrodes. The mechanism of the cerebral response irradiating to the frontal lobes deserves further study. The increase in latency of the irradiation potentials with increasing dis. tahoe from the o~ipital areas suggests that transeortieal irradiation from the visual cortex has a dominant role in this phenomenon. This conjecture is in agreement with the experimental data of Hunter and lngvar (1955) on the irradiated responses to photic stimulation combined with subconvulsive doses of Metrazol. Whether the present results can be applied to all oculoeloni¢ responses with photic stimulation must still be determined. However, it appears that from the demonstration in conventional scalp recordings of the electro. myographi¢ and electro-oculographic concomitants of oculoclonus the absence of a simultaneous frontal irradiation of cortical evoked g~tentials cannot be inferred. SUMMARY Simultaneous deep and supefikial electrograms recorded in two patients with typical "photo.o~ulocloni¢ response" ("fronto.polar recruiting response" of Gastaut or "photo.myoclonic response" of Bickford) suggest that the response consisted in these cases of several recordable components. Surface recordings contained potentials es. sentially muscular and ocular in origin whereas depth electrograms revealed long latency frontal irradiation potentials. No definite clinical diagnostic significance is attributed to the phenomenon of frontal irradiation of visual responses in the human.
REFERENCES BiCI~ORD, R. C. and DALY, D. Experiences with photometrazol test. Electroenceph. clin. Neuropbysiol., 1951, 3: 378. BICKrOP.D,R. G., SEM-JAcoBsEN,G. W., Wsrre, P. T. and D^LY, D. Some observations on the mechanism of photic and Photo-Metrazol activation. Electroenceph. clin. Neurophysiol., 1952, 4: 275-282. BICKFORD,R. G., WHITE,P. T., SEM-JAcoasEN,C. W. and RODIN, E. A. Components of the photomyoclonic response in man. Fed. Prec., 1953, 12: 15-16. CHATRIAN, G. E., POLLACK,C. S. and PETEasEN, M. C. A procedure for preparing a multielectrode lead for intracerebral recordings. F.lectroenceph. clin. Neuro. physiol., 1959, 11: 358-361. G~TAtrr, H. Combined photic and Metrazol activation of the brain. Electroenceph. cli.,~. Ne~7,hvsiol., 1950a, 2: 249--261. G~TAtn, H. Un signe 61ectroenc~phalographique des hydroc~phalies: la r6ponse par recrutement au cours de la stimulation lumineuse intermittente. Rev. neurol., 19g0b, 82: 410-413. GASTAUT,H. Lea deux types de r6ponses photiques irra. di6es chez I'homme. La d~barge myoclonique hyper. syn0hrone et la d~charge myoclonique par recrute. ment. Riv. Neurol., 1951, 21: 27-37. GAST^UT,H. L'activation photo-eardiazolique. Electroen. eeph. ella. Neurophysiol., 1952, 4: 271-274. GASTAUT, H. et COt~RmL, J. Note pr~liminaire sur un proc~16 nouveau et particuli6rement eliicace de stimulation lumineuse intermittente. Eleetroenceph. din. Neurophyslol., 19aJI, 3: 87-88. GASTAUT,H. and HUN~R, J. An experimental study of the mechanism of photi¢ activation in idiopathic
epilep#y. £1ectroeneepk. eBn. Neuropkyslol., ~19'30,2: 263-287. GASTAUT,H,, NAQUL'T,R. et Rooee, A. Cycle d'excitabi. lit6 du cortex frontal au cours de la r6ponse irradi~e photique chez le chat. C.R. Soc. Biol. (Palb), 1951, 145: 1339-1340. H U N ~ , J. and INOVAtX, D. H, Pathways mediating metrazol induced irradiation of visual impulses. £1ee. troenceph, din. Neurophysiol., l~J& 7: 39-60. JOHNSON, D. A. and BICKeOt~D,g. G. Factors affecting cortical, subcortical and myoclonic responses to photic stimulation in cats. £1ectroeneeph. din. NeurophysioL, 1953, 5: 126. RI[MOND, A. In SYtOO#IUM, Photo.Metrazol activation of the EEG. Discussion. £1eetroeneeph. elin. NeurophysloL, 1952, 4: 303--310. SYMPOSIUM.Photo-Metraxol activation of the EEG. Dis-" cussion. £1eetroenceph. din. Neurophy.ffol., 1952, 4: 303-310.
Reference: CHATRIAN,O. E. and PEREZ-BOP.JA,C. Depth electrographic observations in two cases of photo-oculoclonie response. Eleetroenceph. clin. Neurophyslol., 1964, 17: 71-75.