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Non-invasive recording of limbic spindles in man
539
Electroencephalography and Clinical Neurophysiology, 1975, 38:539-541 ,~ Elsevier Scientific Publishing Company, Amsterdam Printed in The Netherlands
LABORATORY NON-INVASIVE
NOTE RECORDING
OF LIMBIC SPINDLES
IN MAN
MARTIN REITE 1 EEG Laboratory, Colorado Psychiatric Hospital, University of Colorado Medical Center, 4200 East Ninth Avenue, Denver, Colo. 80220 (U.S.A.)
(Accepted for publication: December 6, 1974)
Olfactory and/or respiratory related amygdala spindling, a common finding in lower animals, has been recorded with depth electrodes in both chimpanzee (Reite etaL 1967; Adey 1970; Delgado et al. 1970) and man (Lesse et aL 1955; Hughes 1971; Galin, personal communication). In the chimpanzee this activity has been additionally thought to have some relationship to the emotional state of the animal (Reite et al. 1967). Previously thought to be accessible only to depth electrode techniques, we recently reported recording spindling activity in nasopharyngeal recordings from several human subjects, whose morphology and time of occurrence was identical with the spindling recorded from depth electrodes (Reite and Woods 1974), suggesting that this characteristic "depth" activity could be investigated utilizing non-invasive recording techniques. This paper is an extension of our original report. and includes data obtained from nasopharyngeal recordings during the period 1972 1974. METHODS Nasopharyngeal (NP) recordings were obtained from 61 subjects, 8 female and 53 male. Subjects were recorded in the EEG Laboratory of the Colorado Psychiatric Hospital, University of Colorado Medical Center. All recordings were obtained as part of a psychiatric evaluation, most involving a legal sanity determination. The subjects' ages ranged from 14 to 7l years (mean 28.2). All EEGs were recorded on an 8channel Grass Model, 6 EEG machine. Gold disc electrodes were applied according to the International 10-20 placement system; NP electrodes were inserted using the technique described by Mavor and Hellen (1964) 2. Vistaril (50-125 mg) or Seconal (100 mg) sedation was used to help induce sleep in most cases, and sleep (slow wave) recordings were obtained in 44 subjects. Respiration was recorded from most subjects using a Grass Model PT 5A volumetric pressure transducer attached to a bellows strapped around the thorax.
Supported by NIMH Research Scientist Development Award, Type 1, No. 5 K01 MH46335. 2 NP electrodes were obtained from the Electrographic Laboratory Equipment Co., P.O. Box 645, Rochester, Minn. 55901.
RESULTS Well-defined NP spindling activity was recorded in 9 subjects (ages 14-44, mean 24.6). Spindling was present during sleep in 7, during drowsiness in l, and during the waking state in 1. In 8 of the 9 subjects the EEG was otherwise normal; 1 subject had a focal temporal spike abnormality. Six of the 9 subjects had clinical diagnoses of a personality or character disorder. Table I lists pertinent information concerning these 9 subjects. The frequency of the spindling activity ranged from 20 to 28 c/sec. In all cases in which respiration was simultaneously recorded, the spindle bursts coincided with the end of inspiration and/or beginning of expiration. Spindle burst amplitude was less than 50/~V. Maximum amplitude was recorded from the left electrode in 3 subjects, from the right in 2, left and right were equal in 3 cases, and maximum amplitude was between the NP electrodes in 1. There was no apparent association with handedness of the subject. Eight additional subjects had irregular (usually faster) spindle-like activity in NP leads associated with movement or respiration artifact: these will not be considered further. Fig. l illustrates the spindling activity in Subject 5 during light sleep. In this case, spindle frequency was about 22 c/sec, the bursts were about 0.75 sec in duration, and correspond
PG2-PGI - - ~ " " - "
........
~ ..................... " ~
T5-C5 T4-CZ T3-CZ
RESP ~ J -
.... ......... ................ / / ~ - - " ~'°
Fig. I. Nasopharyngeal spindling in a 34-year-old male during light sleep. PG2, right nasopharyngeal electrode. PG I. left nasopharyngeal electrode. Inspiration is up on the respiration recording in bottom channel. Time calibration is I sec.
540
M. Rt-I I !
FABt.E I Details on the 9 subjects exhibiting nasopharyngeal spindling Subiect
Age Sex
[landed- Side of m a x ness amplitude
Spindles awake or asleep
Major Frequency,
Correlation with respiration
Sedali,m
EEG interprelalion
Clinical diagnosis
(I)
18
M
R
R ~ l_
Asleep
28 c;sec
Beginning of expiration
Vislaril ~5 mg
Normal
Antisocial personality
(2)
14
M
R
1 > R
.Asleep
24c,sec
Respiration not recorded
None
Normal
I tysterical neurosis
(1)
22
M
R
Between
Asleep
24 c,sec
Rcspiralion nol recorded
Vistarii, Ic~0 mg
Norntal
Beginning of expiration
",~onc
[41
18
~
R
L-R
20 2 5 c s e c
(51
34
M
R
R=L
Asleep
22 c s e c
End inspiration, begin expiration
{61
26
M
R
I.. = R
Asleep
24 c,sec
(7)
27
M
1.
L= R
Awake
iS)
44
M
R
R > 1.
ft))
IX
M
R
L> R
Nolle
Vislaril. I ~ me
Normal
None
Beginning of expiration
None
Normal
Passive aggressive personality. narcol ic addiction
26 c/se,,"
Beginning of expiration
Secona[. 1I)0 ntg
Normal
Sociopathic personality
Drowsy
24 c/see
End inspiration. begin expiration
Seconal. 100 mg
Normal
Sociopathic personality
Asleep
24 c,sec
Mid expiration
Seconal. I00 lllt2
Normal
Antisocial personalit.~
in time with the beginning ol" expiration. Fig. 2 illustrate,, the periodic occurrence of this spindling activity in Subject 2. a 14-year-old male, over 30 consecutive seconds of recording time. Respiration was not recorded in this subject. In those subjects exhibiting spindling activity, it was not present throughout the recording, but rather would usually appear for periods of a minute or two during the sleep record unaccompanied by any other obvious behavioral or electrographic change.
at"""
PG 1 - T 3
--
-
-%
".+
" poral spike t o c a- , l, , t e l' n
1'4- PG2 P¢;2- p(;1 - -
l)assixe
aggressive
.
.
DISCUSSION
Fig. 2. Thirty consecutive seconds of three channels of EEG data from a 14-year-old male during deep {Stage 4) sleep. The three EEG channels are continuous in time for 3 consecutive l0 sec epochs. Spindling is seen mainly in the left nasopharyngeal electrode (PG1) and between the electrodes (PG2 PG1). Calibration marks are I sec and 50 FtV.
We are unaware of previous published reports of NP spindling activity, although Faur+ (1948) published an illustration of a 22-24 cisec spindle burst recorded from NP electrodes which he thought related to sleep spindle-like activity emanating from the base of the brain. In retrospect. it appears likely that this represented limbic spindling of the type we are describing. The evidence in support of this spindling activity being a real phenomenon is s t r o n g We know that the identical activity is present in the medial amygdala in both m a n and chimpanzee. Both h u m a n and chimpanzee depth recordings
541
LIMBIC SPINDLES IN MAN have demonstrated its amplitude to be quite high (200-300 #V). Several studies have shown that the tips of well-placed NP electrodes lie nearest the uncus, at a distance of about 2 cm (MacLean and Arellano 1950; Rovit et al. 1960; Mavor and Hellen 1964); it would be unreasonable to suppose that high voltage spindling activity occurring in those CNS structures closest to the NP electrode tips would not be visible to those electrodes. The precise anatomical origin of this activity is not certain. Human depth recordings suggest it is found in medial amygdala regions (Galin et al., personal communication), and depth recordings of the homologous activity in the chimpanzee further localize the origin to the uncal cortex overlying the medial amygdala (Reite et al. 1967). Thus, it seems likely that the activity actually arises in the cortex overlying the medial amygdala, and that its detection by more laterally placed amygdala depth electrodes, or the more medial NP electrodes, represents volume conduction from this cortical field. It is hoped that the demonstration that this limbic rhythmicity is, at least in some human subjects, accessible to noninvasive recording techniques will facilitate more detailed investigations of the phenomenon so that its nature and significance might be better understood. SUMMARY Nasopharyngeal (NP) EEG recordings were performed in 61 subjects, ages 14-71 years. Nine subjects exhibited respiration-related spindling activity in the NP electrodes, usually during slow wave sleep. This spindling activity is thought to originate in the cortex overlying the medial amygdala. Previously recorded only with depth electrodes, its appearance in NP recordings indicates that it is accessible to non-invasive recording techniques. RESUME ENREGISTREMENT DES FUSEAUX LIMBIQUES CHEZ L'HOMME PAR UNE METHODE NON PENETRANTE Les enregistrements EEG naso-pharyng6s ont 6t~ r6alis6s chez 61 sujets, ~,g6s de 14/l 71 ans. 9 sujets ont montr6 une
activit6 en fuseaux li6e ii la respiration au niveau des 61ectrodes naso-pharyng6es, habituellement au cours du sommeil'/l ondes lentes. Cette activit6 en fuseaux est suppos6e prendre son origine dans le cortex qui recouvre l'amygdale m6diane. Enregistr6e pr6cedemmentuniquement au moyen d'61ectrodes profondes, son apparition au niveau des enregistrements nasopharyng6s indique que cette activit6 est accessible fi des techniques d'enregistrement non p6n6trantes. The author gratefully acknowledges the assistance of Mrs. Eleanor Totten, who performed most of the EEG examinations reported. REFERENCES ADEY, W. R. Higher olfactory centers. In G. E. W. WOLSTENHOLME and J. KNIGHT (Eds.), Ciba foundation symposium on taste and smell in vertebrates. Churchill, London, 1970: 357-378. DELGADO, J. M. R., JOHNSTON, V. A., WALLACE,J. D. and BRADLEY,R. J. Operant conditioning of amygdala spindling in the free chimpanzee. Brain Res., 1970, 22: 347-362. FAURE,J. Au sujet de l'activit6 de la base du cerveau au cours du sommeil normal et pathologique (d6rivation basale). Rev. neuroL, 1948, 80: 619-621. HUGHES, J. R. Discussion of "Peripheral mechanisms of olfactory discrimination" by P. Macleod. In G. OHLOFF and A. F. THOMAS(Eds.), Gustation andolfaction. Academic Press, London, 1971: 38-41. LESSE, H., HEATH, R. G., MICKLE, W. A., MONROE, R. R. and MILLER, W. H. Rhinencephalic activity during thought. J. nerv. ment. Dis., 1955, 122: 433-440. MACLEAN, P. D. and ARELLANO,A. P. Basal lead studies in epileptic automatisms. Electroenceph. clin. Neurophysiol., 1950, 2: 1-16. MAVOR, H. and HELLEN, M. K. Nasopharyngeal electrode recording. Amer. J. EEG Technol., 1964, 4:43 50. REITE, M., STEPHENS,L. and PEGRAM,G. V. Uncal spindling in the chimpanzee. Brain Res., 1967, 3: 392-395. REITE, M. and WOODS, M. Uncal spindling in man: Nasopharyngeal recordings. Proc. Amer. Soc. Electroenceph. clin. Neurophysiol., 1974, 37: 429. ROVIT, R. R., GLOOR, P. and HENDERSON, L. R. Temporal lobe epilepsy--A study using multiple basal electrodes. I. Description of method. Neurochirurgia ( Stutty. ), 1960, 3: 6-19.
Electroencephalography and Clinical Neurophysiology, 1975, 38:539-541 ,~ Elsevier Scientific Publishing Company, Amsterdam Printed in The Netherlands
LABORATORY NON-INVASIVE
NOTE RECORDING
OF LIMBIC SPINDLES
IN MAN
MARTIN REITE 1 EEG Laboratory, Colorado Psychiatric Hospital, University of Colorado Medical Center, 4200 East Ninth Avenue, Denver, Colo. 80220 (U.S.A.)
(Accepted for publication: December 6, 1974)
Olfactory and/or respiratory related amygdala spindling, a common finding in lower animals, has been recorded with depth electrodes in both chimpanzee (Reite etaL 1967; Adey 1970; Delgado et al. 1970) and man (Lesse et aL 1955; Hughes 1971; Galin, personal communication). In the chimpanzee this activity has been additionally thought to have some relationship to the emotional state of the animal (Reite et al. 1967). Previously thought to be accessible only to depth electrode techniques, we recently reported recording spindling activity in nasopharyngeal recordings from several human subjects, whose morphology and time of occurrence was identical with the spindling recorded from depth electrodes (Reite and Woods 1974), suggesting that this characteristic "depth" activity could be investigated utilizing non-invasive recording techniques. This paper is an extension of our original report. and includes data obtained from nasopharyngeal recordings during the period 1972 1974. METHODS Nasopharyngeal (NP) recordings were obtained from 61 subjects, 8 female and 53 male. Subjects were recorded in the EEG Laboratory of the Colorado Psychiatric Hospital, University of Colorado Medical Center. All recordings were obtained as part of a psychiatric evaluation, most involving a legal sanity determination. The subjects' ages ranged from 14 to 7l years (mean 28.2). All EEGs were recorded on an 8channel Grass Model, 6 EEG machine. Gold disc electrodes were applied according to the International 10-20 placement system; NP electrodes were inserted using the technique described by Mavor and Hellen (1964) 2. Vistaril (50-125 mg) or Seconal (100 mg) sedation was used to help induce sleep in most cases, and sleep (slow wave) recordings were obtained in 44 subjects. Respiration was recorded from most subjects using a Grass Model PT 5A volumetric pressure transducer attached to a bellows strapped around the thorax.
Supported by NIMH Research Scientist Development Award, Type 1, No. 5 K01 MH46335. 2 NP electrodes were obtained from the Electrographic Laboratory Equipment Co., P.O. Box 645, Rochester, Minn. 55901.
RESULTS Well-defined NP spindling activity was recorded in 9 subjects (ages 14-44, mean 24.6). Spindling was present during sleep in 7, during drowsiness in l, and during the waking state in 1. In 8 of the 9 subjects the EEG was otherwise normal; 1 subject had a focal temporal spike abnormality. Six of the 9 subjects had clinical diagnoses of a personality or character disorder. Table I lists pertinent information concerning these 9 subjects. The frequency of the spindling activity ranged from 20 to 28 c/sec. In all cases in which respiration was simultaneously recorded, the spindle bursts coincided with the end of inspiration and/or beginning of expiration. Spindle burst amplitude was less than 50/~V. Maximum amplitude was recorded from the left electrode in 3 subjects, from the right in 2, left and right were equal in 3 cases, and maximum amplitude was between the NP electrodes in 1. There was no apparent association with handedness of the subject. Eight additional subjects had irregular (usually faster) spindle-like activity in NP leads associated with movement or respiration artifact: these will not be considered further. Fig. l illustrates the spindling activity in Subject 5 during light sleep. In this case, spindle frequency was about 22 c/sec, the bursts were about 0.75 sec in duration, and correspond
PG2-PGI - - ~ " " - "
........
~ ..................... " ~
T5-C5 T4-CZ T3-CZ
RESP ~ J -
.... ......... ................ / / ~ - - " ~'°
Fig. I. Nasopharyngeal spindling in a 34-year-old male during light sleep. PG2, right nasopharyngeal electrode. PG I. left nasopharyngeal electrode. Inspiration is up on the respiration recording in bottom channel. Time calibration is I sec.
540
M. Rt-I I !
FABt.E I Details on the 9 subjects exhibiting nasopharyngeal spindling Subiect
Age Sex
[landed- Side of m a x ness amplitude
Spindles awake or asleep
Major Frequency,
Correlation with respiration
Sedali,m
EEG interprelalion
Clinical diagnosis
(I)
18
M
R
R ~ l_
Asleep
28 c;sec
Beginning of expiration
Vislaril ~5 mg
Normal
Antisocial personality
(2)
14
M
R
1 > R
.Asleep
24c,sec
Respiration not recorded
None
Normal
I tysterical neurosis
(1)
22
M
R
Between
Asleep
24 c,sec
Rcspiralion nol recorded
Vistarii, Ic~0 mg
Norntal
Beginning of expiration
",~onc
[41
18
~
R
L-R
20 2 5 c s e c
(51
34
M
R
R=L
Asleep
22 c s e c
End inspiration, begin expiration
{61
26
M
R
I.. = R
Asleep
24 c,sec
(7)
27
M
1.
L= R
Awake
iS)
44
M
R
R > 1.
ft))
IX
M
R
L> R
Nolle
Vislaril. I ~ me
Normal
None
Beginning of expiration
None
Normal
Passive aggressive personality. narcol ic addiction
26 c/se,,"
Beginning of expiration
Secona[. 1I)0 ntg
Normal
Sociopathic personality
Drowsy
24 c/see
End inspiration. begin expiration
Seconal. 100 mg
Normal
Sociopathic personality
Asleep
24 c,sec
Mid expiration
Seconal. I00 lllt2
Normal
Antisocial personalit.~
in time with the beginning ol" expiration. Fig. 2 illustrate,, the periodic occurrence of this spindling activity in Subject 2. a 14-year-old male, over 30 consecutive seconds of recording time. Respiration was not recorded in this subject. In those subjects exhibiting spindling activity, it was not present throughout the recording, but rather would usually appear for periods of a minute or two during the sleep record unaccompanied by any other obvious behavioral or electrographic change.
at"""
PG 1 - T 3
--
-
-%
".+
" poral spike t o c a- , l, , t e l' n
1'4- PG2 P¢;2- p(;1 - -
l)assixe
aggressive
.
.
DISCUSSION
Fig. 2. Thirty consecutive seconds of three channels of EEG data from a 14-year-old male during deep {Stage 4) sleep. The three EEG channels are continuous in time for 3 consecutive l0 sec epochs. Spindling is seen mainly in the left nasopharyngeal electrode (PG1) and between the electrodes (PG2 PG1). Calibration marks are I sec and 50 FtV.
We are unaware of previous published reports of NP spindling activity, although Faur+ (1948) published an illustration of a 22-24 cisec spindle burst recorded from NP electrodes which he thought related to sleep spindle-like activity emanating from the base of the brain. In retrospect. it appears likely that this represented limbic spindling of the type we are describing. The evidence in support of this spindling activity being a real phenomenon is s t r o n g We know that the identical activity is present in the medial amygdala in both m a n and chimpanzee. Both h u m a n and chimpanzee depth recordings
541
LIMBIC SPINDLES IN MAN have demonstrated its amplitude to be quite high (200-300 #V). Several studies have shown that the tips of well-placed NP electrodes lie nearest the uncus, at a distance of about 2 cm (MacLean and Arellano 1950; Rovit et al. 1960; Mavor and Hellen 1964); it would be unreasonable to suppose that high voltage spindling activity occurring in those CNS structures closest to the NP electrode tips would not be visible to those electrodes. The precise anatomical origin of this activity is not certain. Human depth recordings suggest it is found in medial amygdala regions (Galin et al., personal communication), and depth recordings of the homologous activity in the chimpanzee further localize the origin to the uncal cortex overlying the medial amygdala (Reite et al. 1967). Thus, it seems likely that the activity actually arises in the cortex overlying the medial amygdala, and that its detection by more laterally placed amygdala depth electrodes, or the more medial NP electrodes, represents volume conduction from this cortical field. It is hoped that the demonstration that this limbic rhythmicity is, at least in some human subjects, accessible to noninvasive recording techniques will facilitate more detailed investigations of the phenomenon so that its nature and significance might be better understood. SUMMARY Nasopharyngeal (NP) EEG recordings were performed in 61 subjects, ages 14-71 years. Nine subjects exhibited respiration-related spindling activity in the NP electrodes, usually during slow wave sleep. This spindling activity is thought to originate in the cortex overlying the medial amygdala. Previously recorded only with depth electrodes, its appearance in NP recordings indicates that it is accessible to non-invasive recording techniques. RESUME ENREGISTREMENT DES FUSEAUX LIMBIQUES CHEZ L'HOMME PAR UNE METHODE NON PENETRANTE Les enregistrements EEG naso-pharyng6s ont 6t~ r6alis6s chez 61 sujets, ~,g6s de 14/l 71 ans. 9 sujets ont montr6 une
activit6 en fuseaux li6e ii la respiration au niveau des 61ectrodes naso-pharyng6es, habituellement au cours du sommeil'/l ondes lentes. Cette activit6 en fuseaux est suppos6e prendre son origine dans le cortex qui recouvre l'amygdale m6diane. Enregistr6e pr6cedemmentuniquement au moyen d'61ectrodes profondes, son apparition au niveau des enregistrements nasopharyng6s indique que cette activit6 est accessible fi des techniques d'enregistrement non p6n6trantes. The author gratefully acknowledges the assistance of Mrs. Eleanor Totten, who performed most of the EEG examinations reported. REFERENCES ADEY, W. R. Higher olfactory centers. In G. E. W. WOLSTENHOLME and J. KNIGHT (Eds.), Ciba foundation symposium on taste and smell in vertebrates. Churchill, London, 1970: 357-378. DELGADO, J. M. R., JOHNSTON, V. A., WALLACE,J. D. and BRADLEY,R. J. Operant conditioning of amygdala spindling in the free chimpanzee. Brain Res., 1970, 22: 347-362. FAURE,J. Au sujet de l'activit6 de la base du cerveau au cours du sommeil normal et pathologique (d6rivation basale). Rev. neuroL, 1948, 80: 619-621. HUGHES, J. R. Discussion of "Peripheral mechanisms of olfactory discrimination" by P. Macleod. In G. OHLOFF and A. F. THOMAS(Eds.), Gustation andolfaction. Academic Press, London, 1971: 38-41. LESSE, H., HEATH, R. G., MICKLE, W. A., MONROE, R. R. and MILLER, W. H. Rhinencephalic activity during thought. J. nerv. ment. Dis., 1955, 122: 433-440. MACLEAN, P. D. and ARELLANO,A. P. Basal lead studies in epileptic automatisms. Electroenceph. clin. Neurophysiol., 1950, 2: 1-16. MAVOR, H. and HELLEN, M. K. Nasopharyngeal electrode recording. Amer. J. EEG Technol., 1964, 4:43 50. REITE, M., STEPHENS,L. and PEGRAM,G. V. Uncal spindling in the chimpanzee. Brain Res., 1967, 3: 392-395. REITE, M. and WOODS, M. Uncal spindling in man: Nasopharyngeal recordings. Proc. Amer. Soc. Electroenceph. clin. Neurophysiol., 1974, 37: 429. ROVIT, R. R., GLOOR, P. and HENDERSON, L. R. Temporal lobe epilepsy--A study using multiple basal electrodes. I. Description of method. Neurochirurgia ( Stutty. ), 1960, 3: 6-19.