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Uncal spindling in the chimpanzee
392
SHORT COMMUNICATIONS
Uncal spindling in the chimpanzee The exact role of the uncus has not been defined. For some years it has been considered part of the olfactory system, although functionally its relationship to olfaction in primates remains obscure. Pribram and Kruger include it in their conceptualization as part of the second rhinal system, although it may, at least in its anterior aspect, receive fibres directly from the olfactory bulb through the lateral olfactory stria7, 9. Electrical stimulation of the uncus in primates has led to consistent alterations in respiration, usually inhibition or arrest in the expiratory phase 3-6. It has not been possible, however, to record electrical patterns from the uncus that are temporally related to respiration 1,3. With uncal stimulation in man one also finds alterations in the state of consciousness, and the psychic phenomena accompanying 'uncinate fits' have long been known2, 5. Recent work in the chimpanzee has suggested a major role for other nearby limbic structures during paradoxical sleep 8. Three young chimpanzees (17-25 kg) were implanted with chronic depth electrodes, the placements for the most part being different, with the exception of the left uncus which had an electrode located at the same stereotaxic coordinates in all three animals. Cortical recordings were by means of stainless steel skull screws overlying the frontal, frontocentral, parietal, and occipital cortex*. A recurrent and characteristic rhythmical activity was noted in recordings from the uncus of all three animals which, although demonstrating individual differences, was sufficiently similar in all animals to suggest a common underlying mechanism. The first chimpanzee was implanted 9 July 1965. Recording was begun on the fifth postoperative day at which time the uncal activity was first noted. Bursts of 23 c/set spindling activity occurred with a regular periodicity, each burst lasting from 0.5 to 1 sec. The activity begins at the very end of inspiration or beginning of expiration, persists part way through expiration, and subsides before the onset of the next inspiration. Of interest is the fact that this spindling activity is most pronounced while the animal is upset or angry, as in Fig. 1, top. Fig. 1, bottom, was taken from the record 19 min later, and a marked diminution of the spindling is noted although the animal is still alert. The presence of a variety of odors in the inspired air, including banana, orange, apple, benzene, spirits of ammonia, chloroform, dimethylsulfoxide, and ether, was not related to the spindling activity unless the animal actively sniffed, such sniffs being followed by spindle bursts irrespective of the odor, or apparent lack of odor, of the object sniffed. Uncal spindling was not prominent during any stage of sleep with this animal, but was intermittently present during drowsiness. The second animal was implanted 3 August 1965. This animal was involved in an experiment which included continuous monitoring of the electroencephalogram, as well as other physiological measures, for a period of 8 days and nights. During this time background activity from the uncus was similar to that recorded from the other animals, with the excel~tion of being of higher voltage. Rhythmicity at 20-23 c/sec was rare during the awake state, and seen only occasionally during stages 2 to 4 sleep. * The other two animals are currently in other programs and cannot be sacrificedfor some time. Brain Research, 3 (1966/1967) 392-395
393
SHORT COMMUNICATIONS
IO0/xV RESP EKG I SEC !
I
L UNCUS LC- P ioo~v RESP
I SEC I
!
L UNCUS
I
LC-P
I
Fig. l. Top: Animal No. 259, awake and excited. Bottom: Same animal 19 min later, awake and calm. Inspiration is up on the respiratory trace. Uncal spindling is associated with expiration. RESP, respiration; EKG, electrocardiogram; L UNCUS, left uncus; LC-P, left central to parietal cortex. D u r i n g p a r a d o x i c a l sleep, however, this activity was i n v a r i a b l y p r o m i n e n t as seen in Fig. 2. It was again r e l a t e d to the e x p i r a t o r y phase o f respiration, a n d it subsided i m m e d i a t e l y u p o n t r a n s i t i o n f r o m p a r a d o x i c a l to the a w a k e state (Fig. 2.) The a n i m a l
LF
I
LP
J
RP
I [
L HIPP I I
L UNCUS
] L RF I
EOG
op(Nfs~s Fig. 2. Animal No. 157. Prominent uncal spindling is noted during paradoxical sleep. At the arrow the animal opens his eyes and wakens, associated with subsidence of the spindling activity. LF, left frontal cortex; LP, left parietal cortex; RP, right parietal cortex; L HIPP, left hippocampus; L UNCUS left uncus; L RF, left reticular formation; EOG, electrooculogram. Brain Research, 3 0966/1967) 392-395
394
SHORT COMMUNICATIONS
worked a psychomotor program regularly during the 8-day experiment, and shocks administered for incorrect performance, although associated with apparent anger and an increase in the rate and depth of respiration, were not associated with the spindling activity. This animal has since died and it has been possible to obtain histological confirmation of the electrode placement as being in the uncus*. The third animal, implanted 17 August 1965, demonstrates less of this spindling activity than the other two. Spindling was not prominent during the awake state, although with active sniffing bursts of spindling are occasionally recorded. During paradoxical sleep, however, the activity is far more prominent and constant, although slower than in the other two animals, at 20 ~: 1 c/sec. In all animals, regardless of the conditions under which spindling occurs, there is a distinct temporal relation between the spindle bursts and expiration. This can be considered as agreeing with past experiments relating this area to respiration a-6. Since prolonged expiration or respiratory arrest has resulted from stimulation of this area, the spindles might even be a reflection of some inhibitory mechanism. Olfaction, per se, does not seem to play a role of importance, since spindles were not elicited to differing odors unless the animal actively 'sniffed'. In fact, nasal air flow itself was not of importance since spindles did not accompany changes in rate or depth of respiration. From this latter aspect, one might suspect that it was only as the respiratory activity took on biological (i.e., emotional) significance that the spindles were seen. This would not be incompatible with the spindle appearances during paradoxical sleep if one considers 'dreaming' as being an emotive state. In terms of our knowledge of'uncinate fits', which have been described as a 'dreamy state' or 'waking dream', the relation noted may be a lesser example of the pathological type of activity. In summary, the role of the uncus as a part of the olfactory system or the respiratory system may lie in the emotional integration of sensory input. That is, an odor with biological significance may cause uncal activity, in the chimpanzee, that manifests itself behaviorally as a change in respiration. Neurophysiology Section, 6751st Aeromedical Research Laboratory, Holloman Air Force Base, N.Mex., and Department of Psychology, University of New Mexico, Albuquerque, N. Mex. (U.S.A.)
MARTIN REITE LOYD STEPHENS G. VERNON PEGRAM
1 ANGELERI,F., FERRO-MILONE,F., AND PARIGI,S., Electrical activity and reactivity of the rhinen-
cephalic, pararhinencephalic and thalamic structures: Prolonged implantation of electrodes in man. Eleetroenceph. clin. Neurophysiol., 16 (1964) 100-129. 2 BRAIN,R., Diseases of the Nervous System (5th ed.), Oxford University Press, London, 1955, p. 258. 3 HENRY,C. E., SCOVILLE,W. B., ANDDUNSMORE,R. H., Electrical stimulation and recording from the uncus and orbital brain in man. Electroenceph. clin. NeurophysioL, 2 (1950) 357. 4 KAADA,B. R., PRIBRAM,K. H., ANDEPSTEIN,J. A., Respiratory and vascular responses in monkeys from temporal pole, insula, orbital surface and cingulate gyrus. J. NeurophysioL, 12 (1949) 347-356. 5 LIBERSON,W. T., SCOVILLE,W. B., ANDDUNSMORE,R. H., Stimulation studies of the prefrontal lobe and uncus in man. Electroenceph. clin. Neurophysiol., 3 (1951) 1-8. * The "Principles of Laboratory Animal Care" set forth by the National Society for Medical Research were observed during this study. Brain Research, 3 (1966 1967) 392-395
SHORT COMMUNICATIONS
395
6 PAMPIGLIONE,G., AND FALCONER,M. A., Electrical stimulation of the hippocampus in man. In Handbook of Physiology, Sect. 1, Neurophysiology (7th ed.), Amer. Physiol. Soc., Washington, D.C., 1960, p. 1391. 7 PRIERAM,K. H., AND KRUGER,L., Functions of the 'olfactory brain', Ann. IV. Y. Acad. Sci., 58 (1954) 109-138. 8 RHODES,J. M., REITE,M. L., BROWN,D., ANDADEY,W. g., Cgrtical-subcortical relationships of the chimpanzee during different phases of sleep, In M. JOUVET(Ed.), Neurophysiologie des Etats de Sommeil, l~ditions du CNRS, Paris, 1965. 9 TREUX,R. C., AND CARPENTER, M. B., StrongandElwyn's Human Neuroanatomy (5th ed.), Williams and Wilkins, Baltimore, 1964. (Re:eived September 9th, 1966)
Brain Research, 3 (1966/1967) 392-395
SHORT COMMUNICATIONS
Uncal spindling in the chimpanzee The exact role of the uncus has not been defined. For some years it has been considered part of the olfactory system, although functionally its relationship to olfaction in primates remains obscure. Pribram and Kruger include it in their conceptualization as part of the second rhinal system, although it may, at least in its anterior aspect, receive fibres directly from the olfactory bulb through the lateral olfactory stria7, 9. Electrical stimulation of the uncus in primates has led to consistent alterations in respiration, usually inhibition or arrest in the expiratory phase 3-6. It has not been possible, however, to record electrical patterns from the uncus that are temporally related to respiration 1,3. With uncal stimulation in man one also finds alterations in the state of consciousness, and the psychic phenomena accompanying 'uncinate fits' have long been known2, 5. Recent work in the chimpanzee has suggested a major role for other nearby limbic structures during paradoxical sleep 8. Three young chimpanzees (17-25 kg) were implanted with chronic depth electrodes, the placements for the most part being different, with the exception of the left uncus which had an electrode located at the same stereotaxic coordinates in all three animals. Cortical recordings were by means of stainless steel skull screws overlying the frontal, frontocentral, parietal, and occipital cortex*. A recurrent and characteristic rhythmical activity was noted in recordings from the uncus of all three animals which, although demonstrating individual differences, was sufficiently similar in all animals to suggest a common underlying mechanism. The first chimpanzee was implanted 9 July 1965. Recording was begun on the fifth postoperative day at which time the uncal activity was first noted. Bursts of 23 c/set spindling activity occurred with a regular periodicity, each burst lasting from 0.5 to 1 sec. The activity begins at the very end of inspiration or beginning of expiration, persists part way through expiration, and subsides before the onset of the next inspiration. Of interest is the fact that this spindling activity is most pronounced while the animal is upset or angry, as in Fig. 1, top. Fig. 1, bottom, was taken from the record 19 min later, and a marked diminution of the spindling is noted although the animal is still alert. The presence of a variety of odors in the inspired air, including banana, orange, apple, benzene, spirits of ammonia, chloroform, dimethylsulfoxide, and ether, was not related to the spindling activity unless the animal actively sniffed, such sniffs being followed by spindle bursts irrespective of the odor, or apparent lack of odor, of the object sniffed. Uncal spindling was not prominent during any stage of sleep with this animal, but was intermittently present during drowsiness. The second animal was implanted 3 August 1965. This animal was involved in an experiment which included continuous monitoring of the electroencephalogram, as well as other physiological measures, for a period of 8 days and nights. During this time background activity from the uncus was similar to that recorded from the other animals, with the excel~tion of being of higher voltage. Rhythmicity at 20-23 c/sec was rare during the awake state, and seen only occasionally during stages 2 to 4 sleep. * The other two animals are currently in other programs and cannot be sacrificedfor some time. Brain Research, 3 (1966/1967) 392-395
393
SHORT COMMUNICATIONS
IO0/xV RESP EKG I SEC !
I
L UNCUS LC- P ioo~v RESP
I SEC I
!
L UNCUS
I
LC-P
I
Fig. l. Top: Animal No. 259, awake and excited. Bottom: Same animal 19 min later, awake and calm. Inspiration is up on the respiratory trace. Uncal spindling is associated with expiration. RESP, respiration; EKG, electrocardiogram; L UNCUS, left uncus; LC-P, left central to parietal cortex. D u r i n g p a r a d o x i c a l sleep, however, this activity was i n v a r i a b l y p r o m i n e n t as seen in Fig. 2. It was again r e l a t e d to the e x p i r a t o r y phase o f respiration, a n d it subsided i m m e d i a t e l y u p o n t r a n s i t i o n f r o m p a r a d o x i c a l to the a w a k e state (Fig. 2.) The a n i m a l
LF
I
LP
J
RP
I [
L HIPP I I
L UNCUS
] L RF I
EOG
op(Nfs~s Fig. 2. Animal No. 157. Prominent uncal spindling is noted during paradoxical sleep. At the arrow the animal opens his eyes and wakens, associated with subsidence of the spindling activity. LF, left frontal cortex; LP, left parietal cortex; RP, right parietal cortex; L HIPP, left hippocampus; L UNCUS left uncus; L RF, left reticular formation; EOG, electrooculogram. Brain Research, 3 0966/1967) 392-395
394
SHORT COMMUNICATIONS
worked a psychomotor program regularly during the 8-day experiment, and shocks administered for incorrect performance, although associated with apparent anger and an increase in the rate and depth of respiration, were not associated with the spindling activity. This animal has since died and it has been possible to obtain histological confirmation of the electrode placement as being in the uncus*. The third animal, implanted 17 August 1965, demonstrates less of this spindling activity than the other two. Spindling was not prominent during the awake state, although with active sniffing bursts of spindling are occasionally recorded. During paradoxical sleep, however, the activity is far more prominent and constant, although slower than in the other two animals, at 20 ~: 1 c/sec. In all animals, regardless of the conditions under which spindling occurs, there is a distinct temporal relation between the spindle bursts and expiration. This can be considered as agreeing with past experiments relating this area to respiration a-6. Since prolonged expiration or respiratory arrest has resulted from stimulation of this area, the spindles might even be a reflection of some inhibitory mechanism. Olfaction, per se, does not seem to play a role of importance, since spindles were not elicited to differing odors unless the animal actively 'sniffed'. In fact, nasal air flow itself was not of importance since spindles did not accompany changes in rate or depth of respiration. From this latter aspect, one might suspect that it was only as the respiratory activity took on biological (i.e., emotional) significance that the spindles were seen. This would not be incompatible with the spindle appearances during paradoxical sleep if one considers 'dreaming' as being an emotive state. In terms of our knowledge of'uncinate fits', which have been described as a 'dreamy state' or 'waking dream', the relation noted may be a lesser example of the pathological type of activity. In summary, the role of the uncus as a part of the olfactory system or the respiratory system may lie in the emotional integration of sensory input. That is, an odor with biological significance may cause uncal activity, in the chimpanzee, that manifests itself behaviorally as a change in respiration. Neurophysiology Section, 6751st Aeromedical Research Laboratory, Holloman Air Force Base, N.Mex., and Department of Psychology, University of New Mexico, Albuquerque, N. Mex. (U.S.A.)
MARTIN REITE LOYD STEPHENS G. VERNON PEGRAM
1 ANGELERI,F., FERRO-MILONE,F., AND PARIGI,S., Electrical activity and reactivity of the rhinen-
cephalic, pararhinencephalic and thalamic structures: Prolonged implantation of electrodes in man. Eleetroenceph. clin. Neurophysiol., 16 (1964) 100-129. 2 BRAIN,R., Diseases of the Nervous System (5th ed.), Oxford University Press, London, 1955, p. 258. 3 HENRY,C. E., SCOVILLE,W. B., ANDDUNSMORE,R. H., Electrical stimulation and recording from the uncus and orbital brain in man. Electroenceph. clin. NeurophysioL, 2 (1950) 357. 4 KAADA,B. R., PRIBRAM,K. H., ANDEPSTEIN,J. A., Respiratory and vascular responses in monkeys from temporal pole, insula, orbital surface and cingulate gyrus. J. NeurophysioL, 12 (1949) 347-356. 5 LIBERSON,W. T., SCOVILLE,W. B., ANDDUNSMORE,R. H., Stimulation studies of the prefrontal lobe and uncus in man. Electroenceph. clin. Neurophysiol., 3 (1951) 1-8. * The "Principles of Laboratory Animal Care" set forth by the National Society for Medical Research were observed during this study. Brain Research, 3 (1966 1967) 392-395
SHORT COMMUNICATIONS
395
6 PAMPIGLIONE,G., AND FALCONER,M. A., Electrical stimulation of the hippocampus in man. In Handbook of Physiology, Sect. 1, Neurophysiology (7th ed.), Amer. Physiol. Soc., Washington, D.C., 1960, p. 1391. 7 PRIERAM,K. H., AND KRUGER,L., Functions of the 'olfactory brain', Ann. IV. Y. Acad. Sci., 58 (1954) 109-138. 8 RHODES,J. M., REITE,M. L., BROWN,D., ANDADEY,W. g., Cgrtical-subcortical relationships of the chimpanzee during different phases of sleep, In M. JOUVET(Ed.), Neurophysiologie des Etats de Sommeil, l~ditions du CNRS, Paris, 1965. 9 TREUX,R. C., AND CARPENTER, M. B., StrongandElwyn's Human Neuroanatomy (5th ed.), Williams and Wilkins, Baltimore, 1964. (Re:eived September 9th, 1966)
Brain Research, 3 (1966/1967) 392-395