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Human hippocampal formation EEG desynchronizes during attentiveness and movement
778
Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 7 7 8 - - 7 8 1 © Elsevier/North-Holland Scientific Publishers, Ltd.
Clinical note HUMAN HIPPOCAMPAL FORMATION EEG DESYNCHRONIZES D U R I N G A T T E N T I V E N E S S A N D M O V E M E N T *~** ERIC HALGREN ***, THOMAS L. BABB and PAUL H. CRANDALL
Brain Research Institute, Reed Neurological Research Center, and Department of Surgery (Neurological), University of California, Los Angeles, Calif. 90024 (U.S.A.) (Accepted for publication: December 6, 1977)
A classical finding of electroencephalography holds that, in general, the neocortical EEG, recorded in humans or in animals, is desynchronized during alert wakefulness and during paradoxical sleep (PS), and synchronized during slow-wave sleep (Dongier et al. 1976). In contrast, the hippocampal EEG has been reported in animals to be dominated by rhythmic slow activity (RSA, also known as the 'theta rhythm') during certain periods when the animal is highly alert. In the cat, RSA is present during attentive periods (Bennett 1975; Coleman and Lindsley 1975; Kemp and Kaada 1976), and in the rat, during 'voluntary' movements (Vanderwolf 1969; Vanderwolf et al. 1973). In all mammals so far examined, PS is also characterized by hippocampal RSA (Winson 1975). We are reporting elsewhere (Halgren et al., submitted for publication) the changes in human hippocampal unit activity recorded during tasks requiring a variety of movements (9 patients) or attention (15 patients), and during nocturnal sleep sessions including PS (14 patients). These patients suffered from temporal lobe epilepsy, with the result that the hippocampal EEG often exhibited spikes and slow waves. However, in those cases in which the hippocampal EEG lacked gross abnormalities, visual inspection failed to reveal RSA during movement, attentiveness, or PS. Rather, in contrast to what is observed in animals, the human hippocampal EEG showed a * Address reprint requests to: Dr. Eric Halgren, Reed Neurological Research Center, University of California, Los Angeles, Calif. 90024, U.S.A. ** Supported by U.S. Public Health Service Grant NS 02808. *** Supported by the Bank of America--Giannini Foundation and the Ralph Smith Foundation. t The experiments were approved by the Human Subjects Protection Committee of this School of Medicine under guidelines established by the National Institutes of Health. Patients were fully informed of the steps in the research procedures both during interviews and in explicit written form.
desynchronized pattern similar to that simultaneously recorded from the neocortex. We report here a single case in which, as a result of abnormal rhythmic slow waves in the resting EEG, desynchronization during difficult tasks was especially apparent.
Methods Electrodes were chronically implanted in the medial temporal lobes bilaterally, in order to lateralize the seizure focus t . The patient (No. 89 of the Clinical Neurophysiology Program (CNP) series) was a 24-year-old male, who performed within the normal range of intelligence tests and gave no evidence of gross psychopathology. During his spontaneous clinical seizures, abnormal electrographic activity appeared first in the right posterior hippocampus and hippocampal gyrus. Patient selection and electrode implantation techniques have been reported in detail elsewhere (Crandall et al. 1963; Babb and Crandall 1976). The recordings reported in this paper were obtained from 40pro diameter wires stereotaxically placed within the hippocampus and hippocampal gyrus. The fine wires were referred to orthopedic nails, insulated except for their tips, placed into the outer table of the skull at Cz and F z (midline), and shorted together. Since the output impedance of the skull nails in tissue (approximately 1000 ~ ) was far less than that of the fine wires (approx. 400 k ~ ) , and because the nails were in non-neural tissue at a distance from EEG generators, these recordings can be considered essentially unipolar. The EEG recorded by fine wires is closely comparable in quality and content to the EEG that may be simultaneously recorded from the same area by macroelectrodes. Placement was confirmed by X-ray with approximately 88% accuracy according to histological examination of excised lobes from 13 patients of this series (Halgren et al. 1978). Electrodes in the hippocampal gyrus usually terminated within the entorhinal cortex, and the hippocampal electrodes could
HUMAN HIPPOCAMPAL EEG
779
terminate in any of the fields of A m m o n ' s horn, or in the dentate gyrus.
experimenter's hand movements, but synchronized when he tensed all his muscles or made simple alternating hand movements. The EEG was desynchronized when he verbally described his ward or when he silently examined a picture, a n d more synchronized when he described what he had done the previous evening. Hyperventilation was associated with EEG synchronization. These examples, and a detailed examination of the EEG recordings, suggest that the degree of desynchronization was related to the amount of mental effort required by a task. For example, on successive trials of learning a list of word pairs (Fig. 1) or a tapping sequence (Fig. 2), the EEG became progressively synchronized as the task became progressively easier, as indicated by increased rapidity of performance and decreased errors. The interview described above occurred on the seventh postoperative day. That night, the neocortical (C4--A1) and bilateral hippocampal formation EEG were recorded during 2 complete sleep cycles. All
Results Fig. 1 displays the hippocampal EEG during an interview eliciting a variety of behaviors and mental phenomena from patient 89. The hippocampal EEG was dominated by 5--6 c/sec slow waves when the patient was quietly resting. During some, but not all, behavioral segments, the EEG desynchronized, suppressing the slow waves. This suppression showed a general correlation with the amount of movement or speech the patient engaged in, or the rapidity of his breathing. However, the suppression could be clearly dissociated from all of these behavioral parameters. For example, the EEG was desynchronized when the patient tied a bow or imitated the
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,2 sec
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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.
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PT 89
Fig. 1. Suppression of a 5 c/see EEG wave in the hippocampal formation during certain behaviors. At the top is shown the EEG from 5 electrodes in the hippocampal formation, together with the EMG, nasal air temperature, and voice, during a representative 74 rain segment of a 200 min interview. The 3 segments marked A, B and C, exhibiting progressive synchronization, are shown below with a 100-fold expanded time base. Examination of the figure shows clear dissociations between the 5 c/see activity and muscle activity, ventilation and speech. On the other hand, the difficulty of the task does seem to be correlated with the amount of suppression. Tasks requiring little or no cognition, such as HYPERVENTILATing or tensing all muscles, did not suppress the 5 c/see wave. Moderately involving situations, such as EATing or reminiscing about the previous evening (LAST NIGHT) evoked moderate suppression. Maximal suppression occurred during such difficult tasks as mentally rotating a board of objects (OBJECT BOARD), identifying places on a map of his ward (WARD MAP), or imitating movements of the hand (HAND IMITATE). A spectral analysis of these EEG changes is shown in Fig. 2. The patient was receiving no medication at the time of this recording, except for a sleeping pill the previous evening (Dalmane, flurazepam HCI, 30 mg).
E. HALNGREN ET AL.
780
sites were dominated by 5 to 6 c/sec slow waves when the patient was lying quietly awake, and also when the patient was falling asleep. More irregular and generally lower frequency waves were present during stages 3 and 4. During mental arithmetic, during recitation of the alphabet in reverse order, and throughout PS, neocortical and the hippocampal EEG were desynchronized.
o
Discussion l,
'
'
'
I
,
,
,
I
,
,
,
I
,
,
,
I
The present study clearly suggests that the hippocampal RSA present during certain behaviors in animals may be lacking in humans. Executing a difficult tapping sequence or tying a bow were associated with hippocampal desynchronization, in direct contrast to the finding (Vanderwolf 1969 ; Vanderwolf et al. 1973) that voluntary movements including manipulations of objects with the forelimbs are associated with hippocampal RSA in rats. Similarly, the cat hippocampal EEG is dominated by RSA during alert looking (orienting, exploring, staring), especially within a novel environment (Bennett 1975; Coleman and Lindsley 1975; Kemp and Kaada 1976), whereas in our patient the hippocampal EEG was desynchronized during alert looking, for example while examining a picture for memorizing. Paradoxical sleep, which is associated with hippocampal RSA in other mammals (Winson 1975), was associated with desynchronization in our patient. The normal patterns of the electrical activity of human hippocampal formation are, of course, unknown. However, the rhythmic 5--6 c/sec activity during quiet wakefulness in the patient reported here was almost certainly abnormal because it has not been seen in the depth leads of other patients, nor in the scalp leads of normal humans. The usefulness of
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I
2
•
,
,
I
6
,
,
,
I
10
,
,
,
I
14
,
,
,
I
18 c/sec
Fig. 2. Two compressed spectral arrays (CSA) showing the suppression during certain behaviors of a 5 c/sec dominant frequency band. Each line of the CSAs represents a power spectrum of a 4 sec EEG epoch (resolution: 0.5 c/sec). Power spectra of successive epochs are plotted above each other (i.e., time's arrow points up). The CSAs were generated by a PDP-12 computer using the EDAS-1 system developed by N. Fleming and R. Bickford at the University of California at San Diego. The top CSA
shows a strong 5 c/sec band recorded in the left posterior hippocampal gyms. The band is present between tasks, when the patient is resting quietly but is suppressed when the patient is imitating positions of the experimenter's hand or chooses a picture which matches a presented composition of forms (OB). The lower array shows the suppression of the 5 c/sec band in the right posterior hippocampus when the patient is examining a photograph to be remembered (PIC MEM) but not when he is finger tapping an easy sequence (TAP EZ; 1--2--3--4--5 . . . ) . A difficult sequence of finger taps ( T A P - H A R D ; 1 - - 5 - - 2 - - 5 - - 3 - - 4 . . . ) suppresses the 5c/sec band when it is first introduced (bottom) but not after it is well learned (top).
HUMAN HIPPOCAMPAL EEG these 5--6 c/sec waves was that they permitted a further desynchronization during difficult tasks to be clearly observed; in other patients in whom the hippocampal EEG was ordinarily desynchronized during quiet wakefulness, it was not possible to identify by visual inspection any EEG changes associated with task difficulty. What was clearly consistent between the case presented here and our other patients was that the human hippocampal EEG desynchronized during behaviors homologous to those accompanied by hippocampal RSA in animals.
781 que l'activit~ lente rythmique ('th~ta') observ~e chez les rats et les chats au cours de comportements sp~cifiques n'est pas observ~e dans la formation hippocampique chez l'homme au cours de comportements homologues. We thank E. Cart, E. Mariani, J. Lieb, and S. Woods for technical assistance, J. Billups and J. Hopgood for typing the manuscript, and Patient 89 for his cooperation.
References Summary The relation of the hippocampal EEG to behavior and to the neocortical EEG is being studied in psychomotor epileptics. Hippocampal recordings displaying only rare epileptiform spikes and slow waves are found to follow grossly the simultaneously recorded neocortical EEG, becoming desynchronized during wakefulness and paradoxical sleep (PS), and displaying large irregular slow waves during slow-wave sleep. In the one patient reported in this clinical note, strong rhythmic 5--6 c/sec waves dominated the neocortical and hippocampal EEG during quiet wakefulness. These slow waves were replaced by desynchronized activity during PS and during difficult tasks, suggesting a further desynchronizing influence. The findings in all patients suggest that the rhythmic slow activity ('theta') found in rats and cats during specific behaviors is not observed in the human hippocampal formation during the homologous behaviors.
R~sum~ Ddsynchronisation de I'EEG de la formation hippocampique chez l'homme au cours de l'attention et du m ouv e men t
La relation entre EEG hippocampique, comportement, et EEG n~o-cortical a 4t~ ~tudi~e chez des 4pileptiques psycho-moteurs. I1 apparaft que les enregistrements hippocampiques qui ne montrent que de rares pointes et ondes lentes paroxystiques suivent en gros I'EEG n~o-cortical enregistr~ simultan~ment, se d~synchronisent au cours de l'~veil et du sommeil paradoxal (PS) et m o n t r e n t de grandes ondes lentes irr4guli~res au cours du sommeil lent. Chez un malade rapport~ dans cette note clinique, de grandes ondes lentes rythmiques ~ 5--6 c/sec dominent I'EEG n~o-cortical et hippocampique au cours de la veille calme. Ces ondes lentes sont remplac~es par une activit~ d~synchronis4e au cours du sommeil paradoxal et au cours de t~ches difficiles, sugg~rant une influence d~synchronisatrice suppl~mentaire. Les donn~es obtenues chez tousles malades m o n t r e n t
Babb, T.L. and Crandall, P.H. Epileptogenesis of human limbic neurons in psychomotor epileptics. Electroenceph. clin. Neurophysiol., 1976, 40: 225--243. Bennett, T.L. The electrical activity of the hippocampus and processes of attention. In: R.L. Isaacson and K.H. Pribram (Eds.), The Hippocampus, Vol. 2. Neurophysiology and Behavior. Plenum Press, New York, 1975: 71--99. Coleman, J.R. and Lindsley, D.B. Hippocampal electrical correlates of free behavior and behavior induced by stimulation of two hypothalamichippocampal systems in the cat. Exp. Neurol., 1975, 49: 506--528. Crandall, P.H., Walter, R.D. and Rand, R.W. Clinical application of studies of stereotactically implanted electrodes in temporal-lobe epilepsy. J. Neurosurg., 1963, 21: 827--840. Dongier, M., McCallum, W.C., Torres, F. and Vogel, W. The EEG of the waking adult. Section III. Psychological and psychophysiological states. In: G.E. Chatrian and G.C. Lairy (Eds.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 6A. Elsevier, Amsterdam, 1976: 195-256. Halgren, E., Walter, R.D., Cherlow, D.G. and Crandall, P.H. Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain, 1978, 101: 83--117. Kemp, I.R. and Kaada, B.R. The relation of hippocampal theta activity to arousal, attentive behavior, and somatomotor movements in unrestrained cats. Brain Res., 1976, 95: 478--486. Vanderwolf, C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. clin. Neurophysiol., 1969, 26: 407--410. Vanderwolf, C.H., Bland, B.H. and Whislaw, I.Q. Diencephalic, hippocampal, and neocortical mechanisms in voluntary movement. I n : J. Maser (Ed.), Efferent Organization and the Integration of Behavior. Academic Press, New York, 1973: 229-262. Winson, J. The 0 mode of hippocampal function. In: R.L. Isaacson and K.H. Pribram (Eds.), The Hippocampus, Vol. 2, Neurophysiology and Behavior. Plenum Press, New York, 1975: 169--183.
Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 7 7 8 - - 7 8 1 © Elsevier/North-Holland Scientific Publishers, Ltd.
Clinical note HUMAN HIPPOCAMPAL FORMATION EEG DESYNCHRONIZES D U R I N G A T T E N T I V E N E S S A N D M O V E M E N T *~** ERIC HALGREN ***, THOMAS L. BABB and PAUL H. CRANDALL
Brain Research Institute, Reed Neurological Research Center, and Department of Surgery (Neurological), University of California, Los Angeles, Calif. 90024 (U.S.A.) (Accepted for publication: December 6, 1977)
A classical finding of electroencephalography holds that, in general, the neocortical EEG, recorded in humans or in animals, is desynchronized during alert wakefulness and during paradoxical sleep (PS), and synchronized during slow-wave sleep (Dongier et al. 1976). In contrast, the hippocampal EEG has been reported in animals to be dominated by rhythmic slow activity (RSA, also known as the 'theta rhythm') during certain periods when the animal is highly alert. In the cat, RSA is present during attentive periods (Bennett 1975; Coleman and Lindsley 1975; Kemp and Kaada 1976), and in the rat, during 'voluntary' movements (Vanderwolf 1969; Vanderwolf et al. 1973). In all mammals so far examined, PS is also characterized by hippocampal RSA (Winson 1975). We are reporting elsewhere (Halgren et al., submitted for publication) the changes in human hippocampal unit activity recorded during tasks requiring a variety of movements (9 patients) or attention (15 patients), and during nocturnal sleep sessions including PS (14 patients). These patients suffered from temporal lobe epilepsy, with the result that the hippocampal EEG often exhibited spikes and slow waves. However, in those cases in which the hippocampal EEG lacked gross abnormalities, visual inspection failed to reveal RSA during movement, attentiveness, or PS. Rather, in contrast to what is observed in animals, the human hippocampal EEG showed a * Address reprint requests to: Dr. Eric Halgren, Reed Neurological Research Center, University of California, Los Angeles, Calif. 90024, U.S.A. ** Supported by U.S. Public Health Service Grant NS 02808. *** Supported by the Bank of America--Giannini Foundation and the Ralph Smith Foundation. t The experiments were approved by the Human Subjects Protection Committee of this School of Medicine under guidelines established by the National Institutes of Health. Patients were fully informed of the steps in the research procedures both during interviews and in explicit written form.
desynchronized pattern similar to that simultaneously recorded from the neocortex. We report here a single case in which, as a result of abnormal rhythmic slow waves in the resting EEG, desynchronization during difficult tasks was especially apparent.
Methods Electrodes were chronically implanted in the medial temporal lobes bilaterally, in order to lateralize the seizure focus t . The patient (No. 89 of the Clinical Neurophysiology Program (CNP) series) was a 24-year-old male, who performed within the normal range of intelligence tests and gave no evidence of gross psychopathology. During his spontaneous clinical seizures, abnormal electrographic activity appeared first in the right posterior hippocampus and hippocampal gyrus. Patient selection and electrode implantation techniques have been reported in detail elsewhere (Crandall et al. 1963; Babb and Crandall 1976). The recordings reported in this paper were obtained from 40pro diameter wires stereotaxically placed within the hippocampus and hippocampal gyrus. The fine wires were referred to orthopedic nails, insulated except for their tips, placed into the outer table of the skull at Cz and F z (midline), and shorted together. Since the output impedance of the skull nails in tissue (approximately 1000 ~ ) was far less than that of the fine wires (approx. 400 k ~ ) , and because the nails were in non-neural tissue at a distance from EEG generators, these recordings can be considered essentially unipolar. The EEG recorded by fine wires is closely comparable in quality and content to the EEG that may be simultaneously recorded from the same area by macroelectrodes. Placement was confirmed by X-ray with approximately 88% accuracy according to histological examination of excised lobes from 13 patients of this series (Halgren et al. 1978). Electrodes in the hippocampal gyrus usually terminated within the entorhinal cortex, and the hippocampal electrodes could
HUMAN HIPPOCAMPAL EEG
779
terminate in any of the fields of A m m o n ' s horn, or in the dentate gyrus.
experimenter's hand movements, but synchronized when he tensed all his muscles or made simple alternating hand movements. The EEG was desynchronized when he verbally described his ward or when he silently examined a picture, a n d more synchronized when he described what he had done the previous evening. Hyperventilation was associated with EEG synchronization. These examples, and a detailed examination of the EEG recordings, suggest that the degree of desynchronization was related to the amount of mental effort required by a task. For example, on successive trials of learning a list of word pairs (Fig. 1) or a tapping sequence (Fig. 2), the EEG became progressively synchronized as the task became progressively easier, as indicated by increased rapidity of performance and decreased errors. The interview described above occurred on the seventh postoperative day. That night, the neocortical (C4--A1) and bilateral hippocampal formation EEG were recorded during 2 complete sleep cycles. All
Results Fig. 1 displays the hippocampal EEG during an interview eliciting a variety of behaviors and mental phenomena from patient 89. The hippocampal EEG was dominated by 5--6 c/sec slow waves when the patient was quietly resting. During some, but not all, behavioral segments, the EEG desynchronized, suppressing the slow waves. This suppression showed a general correlation with the amount of movement or speech the patient engaged in, or the rapidity of his breathing. However, the suppression could be clearly dissociated from all of these behavioral parameters. For example, the EEG was desynchronized when the patient tied a bow or imitated the
.,~.~,
._v~.~
~
LT
MID
HC GYRUS
,2 sec
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
- - ~ - ¢ v ~ - ~ R T
MID
EMG /~',,
~
"~\
~
-~'~
J
,
.
~
_
........
- ~.~
- -
-----
~ N A S A L
VOICE
HC
GYRUS
HAND ÷ CHIN THERMISTOR
PT 89
Fig. 1. Suppression of a 5 c/see EEG wave in the hippocampal formation during certain behaviors. At the top is shown the EEG from 5 electrodes in the hippocampal formation, together with the EMG, nasal air temperature, and voice, during a representative 74 rain segment of a 200 min interview. The 3 segments marked A, B and C, exhibiting progressive synchronization, are shown below with a 100-fold expanded time base. Examination of the figure shows clear dissociations between the 5 c/see activity and muscle activity, ventilation and speech. On the other hand, the difficulty of the task does seem to be correlated with the amount of suppression. Tasks requiring little or no cognition, such as HYPERVENTILATing or tensing all muscles, did not suppress the 5 c/see wave. Moderately involving situations, such as EATing or reminiscing about the previous evening (LAST NIGHT) evoked moderate suppression. Maximal suppression occurred during such difficult tasks as mentally rotating a board of objects (OBJECT BOARD), identifying places on a map of his ward (WARD MAP), or imitating movements of the hand (HAND IMITATE). A spectral analysis of these EEG changes is shown in Fig. 2. The patient was receiving no medication at the time of this recording, except for a sleeping pill the previous evening (Dalmane, flurazepam HCI, 30 mg).
E. HALNGREN ET AL.
780
sites were dominated by 5 to 6 c/sec slow waves when the patient was lying quietly awake, and also when the patient was falling asleep. More irregular and generally lower frequency waves were present during stages 3 and 4. During mental arithmetic, during recitation of the alphabet in reverse order, and throughout PS, neocortical and the hippocampal EEG were desynchronized.
o
Discussion l,
'
'
'
I
,
,
,
I
,
,
,
I
,
,
,
I
The present study clearly suggests that the hippocampal RSA present during certain behaviors in animals may be lacking in humans. Executing a difficult tapping sequence or tying a bow were associated with hippocampal desynchronization, in direct contrast to the finding (Vanderwolf 1969 ; Vanderwolf et al. 1973) that voluntary movements including manipulations of objects with the forelimbs are associated with hippocampal RSA in rats. Similarly, the cat hippocampal EEG is dominated by RSA during alert looking (orienting, exploring, staring), especially within a novel environment (Bennett 1975; Coleman and Lindsley 1975; Kemp and Kaada 1976), whereas in our patient the hippocampal EEG was desynchronized during alert looking, for example while examining a picture for memorizing. Paradoxical sleep, which is associated with hippocampal RSA in other mammals (Winson 1975), was associated with desynchronization in our patient. The normal patterns of the electrical activity of human hippocampal formation are, of course, unknown. However, the rhythmic 5--6 c/sec activity during quiet wakefulness in the patient reported here was almost certainly abnormal because it has not been seen in the depth leads of other patients, nor in the scalp leads of normal humans. The usefulness of
~e z
I
2
•
,
,
I
6
,
,
,
I
10
,
,
,
I
14
,
,
,
I
18 c/sec
Fig. 2. Two compressed spectral arrays (CSA) showing the suppression during certain behaviors of a 5 c/sec dominant frequency band. Each line of the CSAs represents a power spectrum of a 4 sec EEG epoch (resolution: 0.5 c/sec). Power spectra of successive epochs are plotted above each other (i.e., time's arrow points up). The CSAs were generated by a PDP-12 computer using the EDAS-1 system developed by N. Fleming and R. Bickford at the University of California at San Diego. The top CSA
shows a strong 5 c/sec band recorded in the left posterior hippocampal gyms. The band is present between tasks, when the patient is resting quietly but is suppressed when the patient is imitating positions of the experimenter's hand or chooses a picture which matches a presented composition of forms (OB). The lower array shows the suppression of the 5 c/sec band in the right posterior hippocampus when the patient is examining a photograph to be remembered (PIC MEM) but not when he is finger tapping an easy sequence (TAP EZ; 1--2--3--4--5 . . . ) . A difficult sequence of finger taps ( T A P - H A R D ; 1 - - 5 - - 2 - - 5 - - 3 - - 4 . . . ) suppresses the 5c/sec band when it is first introduced (bottom) but not after it is well learned (top).
HUMAN HIPPOCAMPAL EEG these 5--6 c/sec waves was that they permitted a further desynchronization during difficult tasks to be clearly observed; in other patients in whom the hippocampal EEG was ordinarily desynchronized during quiet wakefulness, it was not possible to identify by visual inspection any EEG changes associated with task difficulty. What was clearly consistent between the case presented here and our other patients was that the human hippocampal EEG desynchronized during behaviors homologous to those accompanied by hippocampal RSA in animals.
781 que l'activit~ lente rythmique ('th~ta') observ~e chez les rats et les chats au cours de comportements sp~cifiques n'est pas observ~e dans la formation hippocampique chez l'homme au cours de comportements homologues. We thank E. Cart, E. Mariani, J. Lieb, and S. Woods for technical assistance, J. Billups and J. Hopgood for typing the manuscript, and Patient 89 for his cooperation.
References Summary The relation of the hippocampal EEG to behavior and to the neocortical EEG is being studied in psychomotor epileptics. Hippocampal recordings displaying only rare epileptiform spikes and slow waves are found to follow grossly the simultaneously recorded neocortical EEG, becoming desynchronized during wakefulness and paradoxical sleep (PS), and displaying large irregular slow waves during slow-wave sleep. In the one patient reported in this clinical note, strong rhythmic 5--6 c/sec waves dominated the neocortical and hippocampal EEG during quiet wakefulness. These slow waves were replaced by desynchronized activity during PS and during difficult tasks, suggesting a further desynchronizing influence. The findings in all patients suggest that the rhythmic slow activity ('theta') found in rats and cats during specific behaviors is not observed in the human hippocampal formation during the homologous behaviors.
R~sum~ Ddsynchronisation de I'EEG de la formation hippocampique chez l'homme au cours de l'attention et du m ouv e men t
La relation entre EEG hippocampique, comportement, et EEG n~o-cortical a 4t~ ~tudi~e chez des 4pileptiques psycho-moteurs. I1 apparaft que les enregistrements hippocampiques qui ne montrent que de rares pointes et ondes lentes paroxystiques suivent en gros I'EEG n~o-cortical enregistr~ simultan~ment, se d~synchronisent au cours de l'~veil et du sommeil paradoxal (PS) et m o n t r e n t de grandes ondes lentes irr4guli~res au cours du sommeil lent. Chez un malade rapport~ dans cette note clinique, de grandes ondes lentes rythmiques ~ 5--6 c/sec dominent I'EEG n~o-cortical et hippocampique au cours de la veille calme. Ces ondes lentes sont remplac~es par une activit~ d~synchronis4e au cours du sommeil paradoxal et au cours de t~ches difficiles, sugg~rant une influence d~synchronisatrice suppl~mentaire. Les donn~es obtenues chez tousles malades m o n t r e n t
Babb, T.L. and Crandall, P.H. Epileptogenesis of human limbic neurons in psychomotor epileptics. Electroenceph. clin. Neurophysiol., 1976, 40: 225--243. Bennett, T.L. The electrical activity of the hippocampus and processes of attention. In: R.L. Isaacson and K.H. Pribram (Eds.), The Hippocampus, Vol. 2. Neurophysiology and Behavior. Plenum Press, New York, 1975: 71--99. Coleman, J.R. and Lindsley, D.B. Hippocampal electrical correlates of free behavior and behavior induced by stimulation of two hypothalamichippocampal systems in the cat. Exp. Neurol., 1975, 49: 506--528. Crandall, P.H., Walter, R.D. and Rand, R.W. Clinical application of studies of stereotactically implanted electrodes in temporal-lobe epilepsy. J. Neurosurg., 1963, 21: 827--840. Dongier, M., McCallum, W.C., Torres, F. and Vogel, W. The EEG of the waking adult. Section III. Psychological and psychophysiological states. In: G.E. Chatrian and G.C. Lairy (Eds.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 6A. Elsevier, Amsterdam, 1976: 195-256. Halgren, E., Walter, R.D., Cherlow, D.G. and Crandall, P.H. Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain, 1978, 101: 83--117. Kemp, I.R. and Kaada, B.R. The relation of hippocampal theta activity to arousal, attentive behavior, and somatomotor movements in unrestrained cats. Brain Res., 1976, 95: 478--486. Vanderwolf, C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. clin. Neurophysiol., 1969, 26: 407--410. Vanderwolf, C.H., Bland, B.H. and Whislaw, I.Q. Diencephalic, hippocampal, and neocortical mechanisms in voluntary movement. I n : J. Maser (Ed.), Efferent Organization and the Integration of Behavior. Academic Press, New York, 1973: 229-262. Winson, J. The 0 mode of hippocampal function. In: R.L. Isaacson and K.H. Pribram (Eds.), The Hippocampus, Vol. 2, Neurophysiology and Behavior. Plenum Press, New York, 1975: 169--183.