Brain Research, 134 (1977) 581-584 © Elsevier/North-Holland Biomedical Press
581
Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins L. M. MUKHAMETOV, A. Y. SUPIN and I. G. POLYAKOVA Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Moscow 117071 (U.S.S.R.)
(Accepted June 15th, 1977)
In all mammals investigated the change in patterns of electroencephalogram (EEG) from synchronization to desynchronization and vice versa occurs simultaneously in both hemispheres during sleep-wakefulness cycle. We found that the two brain hemispheres of bottlenose dolphins (Tursiops truncatus) could generate synchronized or desynchronized EEG patterns not only simultaneously but also independently. This unusual interhemispheric asymmetry of the brain functional states was found in the course of systematic electrophysiological investigation of sleep in Black Sea bottlenose dolphins. Only one attempt to study the electroencephalogram during the dolphin's sleep-wakefulness cycle is known up to now a,4, but this work was based on very little experimental data (sleep observation during one night on one pilot whale) and the conclusions made from this single experiment seem to be speculative. It is however interesting, that in this work some signs of an EEG lateralization were observed, too. In the work presented here, the sleep of 9 adult bottlenose dolphins of both sexes was studied during three summer seasons. The dolphins were captured 2~, months before electrode implantation and were not housed specially. Electrodes for recording the electrocorticogram (ECoG), electromyogram (EMG) of neck and eye muscles, electrocardiogram and pneumogram were implanted under local anaesthesia. After novocainization the skin and muscles of the head were penetrated with a steel tube (outer diameter 4 mm) up to the skull bone. A drill inside this tube was used to make a hole through the bone and epi- and intracortical recording electrodes were fixed firmly in the bone aperture 2. Harpoon-shaped E M G electrodes were inserted with the aid of a syringe needle in various neck muscles and extraocular muscles; from these electrodes it was usually possible to record the electrocardiogram and the E M G of breathing movements. Small diameter special artefact-free cables from all ECoG and E M G electrodes were secured by a stainless steel screw inserted in the skull bone 5-7 cm behind the blowhole. They were connected to the input of an 8channel electroencephalograph. Cables were of 6-m length and did not prevent free movements of the animal. During the experiments the dolphin was swimming freely in the tank 5 x 5 x
582 1.2 m. The animal adapted to the tank for up to two months. Continuous polygraphic recordings for up to 72 h were made during several weeks following electrode implantation. The study of evoked potentials revealed that the electrode locations were mainly in the acoustic and visual cortical areas. Anatomical postmortem investigations showed that ECoG electrodes were widely spaced in parietal and occipital cortex. In analysing the ECoG records 3 stages were distinguished: stage t, desynchronization; stage 2, intermediate synchronization including sleep spindles, theta- and delta-waves; stage 3, maximal synchronization when delta-waves of maximal amplitude occupied not less than two-thirds of each scoring epoch (20 sec). Wakefulness (W) and slow sleep (SS) were identified according to usual ECoG criteria. W was characterized by bilateral ECoG desynchronization (stage 1) and SS by bilateral ECoG synchronization (stage 2). We have up to now not observed polygraphic records characteristic of paradoxical sleep (PS). E M G activity in the neck muscles of this aquatic animal can be absent during obvious W as well as during SS. The ECoG, oculomotor EMG, electrocardiogram and pneumogram also failed to reveal the presence of PS. It may be, however, that further parameters for the identification of this stage may be required. In addition to the typical bilateral ECoG synchronization and bilateral desynchronization which has been observed in other mammals, the ECoG patterns of the dolphin show an unusual interhemispheric asymmetry (Figs. 1 and 2). Fig. 1 demonstrates that the unilateral synchronization might appear in all recorded points of one hemisphere simultaneously and, at the same time, ECoG desynchronization in all points of the other hemisphere. In some cases we observed that ECoG synchronization began or ended independently in different points of the same hemisphere. The unilateral ECoG synchronization can appear alternatively in either hemisphere (Fig. 2).
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Fig. 1. Interhemispheric asymmetry of the ECoG sleep patterns of dolphin no. 8. A: electrode localization in parieto-occipital cortex. B and C: prominent ECoG delta-waves in all three points of one hemisphere simultaneously with the ECoG desynchronization in all three points of the other hemisphere. The records C were obtained one hour later than those of B. Unipolar registration.
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~I S AM Fig. 2. Diagram of ECoG stages 1 (desynchronization), 2 (intermediate synchronization) and 3 (maximal synchronization)in left (L) and right (R) hemispheres during two differentnights (A and B) in dolphin no. 9. Bipolar recording from roughly symmetricalareas of the parietal cortex. Time scale in hours. The beginningof diagram A corresponds to the end of feeding; that of diagram B to the end of a 60-h period of total sleep deprivation.
Up to now, stage 3 has only been observed unilaterally. However, bilateral deltawaves of maximal amplitude have been observed during barbiturate narcotization, but only after autonomic respiration stopped. Interhemispheric asymmetry was observed in 6 of 9 investigated animals. In the first three experimental animals this asymmetry was not observed, but this is believed to be because only limited bilateral ECoG records were made with these animals. The male no. 9 had the following total time percentage of sleep-wakefulness stages during a 72-h session: bilateral desynchronization occupied 56.8 ~ ; bilateral synchronization (stages 2 and 2, or 2 and 3) occupied 0.8 ~ ; unilateral synchronization occupied 42.4 ~ of recording time, of which right-side synchronization occupied 14.7 ~ (stage 2, 9.6 ~ and stage 3, 5.1 ~) and left-side synchronization 27.7 ~o (stage 2, 19.1 ~ and stage 3, 8.6 ~o). No behavioural differences were found in our experimental conditions between states characterized by bilateral ECoG synchronization and by unilateral synchronization. The animals were practically immobile in both states. Apart from respiratory movements, the only other small movements visible were of the the fins and fluke, for postural maintenance. During the periods when one eye was open and the other was closed 1 the ECoG synchronization as well as desynchronization might be observed in either hemisphereL It is concluded that the unilaterally synchronized hemisphere is in SS, because the synchronized pattern of the dolphin is so typical of slow-wave activity of all mammals. The unilaterally desynchronized hemisphere is most probably awake. It cannot, however, be excluded that the unilaterally desynchronized hemisphere is in PS, since this phase of sleep is also characterized by ECoG desynchronization, and typical PS has not yet been found in the dolphin. The functional significance of the alternating interhemispheric asymmetry is still unclear. Of possible explanations, the performance of sentinel functions by the unilaterally desynchronized hemisphere, or the impossibility of maintaining respira-
584 tion d u r i n g bilateral delta-sleep, or during bilateral PS, are speculative. The n e u r o p h y siological m e c h a n i s m o f the observed p h e n o m e n o n is also unclear. It is hypothesized t h a t different levels o f activation in the two hemispheres result f r o m functional independence o f the two halves o f some activating or deactivating system in the b r a i n stem.
1 Lilly, J. C., Animal in aquatic environments: adaptation of mammals to the ocean. In D. B. Dill (Ed.), Handbook of Physiology--Environment, John Wiley and Sons, New York, 1964, pp. 741-747. 2 Mukhametov, L. M. and Supin, A. Y., EEG study of different behavioral states in free-moving dolphin (Tursiops truncatus), J. high. nerv. Activ., 25 (1975) 396-401 (in Russian). 3 Serafetinides, E. A., Shurley, J. T. and Brooks, R. E., Electroencephalogram of the pilot whale, Globicephala scammoni, in wakefulness and sleep: lateralization aspects, Int. J. Psychobiol., 2 (1971-1972) 129-135. 4 Shurley, J. T., Serafetinides, E. A., Brooks, R. E., Eisner, R. and Kenney, D. W., Sleep in cetaceans. I. The pilot whale, Globicephala scammoni, Psychophysiology, 6 (1969) 230.
581
Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins L. M. MUKHAMETOV, A. Y. SUPIN and I. G. POLYAKOVA Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Moscow 117071 (U.S.S.R.)
(Accepted June 15th, 1977)
In all mammals investigated the change in patterns of electroencephalogram (EEG) from synchronization to desynchronization and vice versa occurs simultaneously in both hemispheres during sleep-wakefulness cycle. We found that the two brain hemispheres of bottlenose dolphins (Tursiops truncatus) could generate synchronized or desynchronized EEG patterns not only simultaneously but also independently. This unusual interhemispheric asymmetry of the brain functional states was found in the course of systematic electrophysiological investigation of sleep in Black Sea bottlenose dolphins. Only one attempt to study the electroencephalogram during the dolphin's sleep-wakefulness cycle is known up to now a,4, but this work was based on very little experimental data (sleep observation during one night on one pilot whale) and the conclusions made from this single experiment seem to be speculative. It is however interesting, that in this work some signs of an EEG lateralization were observed, too. In the work presented here, the sleep of 9 adult bottlenose dolphins of both sexes was studied during three summer seasons. The dolphins were captured 2~, months before electrode implantation and were not housed specially. Electrodes for recording the electrocorticogram (ECoG), electromyogram (EMG) of neck and eye muscles, electrocardiogram and pneumogram were implanted under local anaesthesia. After novocainization the skin and muscles of the head were penetrated with a steel tube (outer diameter 4 mm) up to the skull bone. A drill inside this tube was used to make a hole through the bone and epi- and intracortical recording electrodes were fixed firmly in the bone aperture 2. Harpoon-shaped E M G electrodes were inserted with the aid of a syringe needle in various neck muscles and extraocular muscles; from these electrodes it was usually possible to record the electrocardiogram and the E M G of breathing movements. Small diameter special artefact-free cables from all ECoG and E M G electrodes were secured by a stainless steel screw inserted in the skull bone 5-7 cm behind the blowhole. They were connected to the input of an 8channel electroencephalograph. Cables were of 6-m length and did not prevent free movements of the animal. During the experiments the dolphin was swimming freely in the tank 5 x 5 x
582 1.2 m. The animal adapted to the tank for up to two months. Continuous polygraphic recordings for up to 72 h were made during several weeks following electrode implantation. The study of evoked potentials revealed that the electrode locations were mainly in the acoustic and visual cortical areas. Anatomical postmortem investigations showed that ECoG electrodes were widely spaced in parietal and occipital cortex. In analysing the ECoG records 3 stages were distinguished: stage t, desynchronization; stage 2, intermediate synchronization including sleep spindles, theta- and delta-waves; stage 3, maximal synchronization when delta-waves of maximal amplitude occupied not less than two-thirds of each scoring epoch (20 sec). Wakefulness (W) and slow sleep (SS) were identified according to usual ECoG criteria. W was characterized by bilateral ECoG desynchronization (stage 1) and SS by bilateral ECoG synchronization (stage 2). We have up to now not observed polygraphic records characteristic of paradoxical sleep (PS). E M G activity in the neck muscles of this aquatic animal can be absent during obvious W as well as during SS. The ECoG, oculomotor EMG, electrocardiogram and pneumogram also failed to reveal the presence of PS. It may be, however, that further parameters for the identification of this stage may be required. In addition to the typical bilateral ECoG synchronization and bilateral desynchronization which has been observed in other mammals, the ECoG patterns of the dolphin show an unusual interhemispheric asymmetry (Figs. 1 and 2). Fig. 1 demonstrates that the unilateral synchronization might appear in all recorded points of one hemisphere simultaneously and, at the same time, ECoG desynchronization in all points of the other hemisphere. In some cases we observed that ECoG synchronization began or ended independently in different points of the same hemisphere. The unilateral ECoG synchronization can appear alternatively in either hemisphere (Fig. 2).
A
B
E
loo ~v
4,,,r,,.,.,/v~~
10 cm
6~
,
'e'~'X-~'''-~'Lh'J
~,"~ ~,, ~,,v~" ~ ' i / , .
,,f' ~,,/" ] 1 see
Fig. 1. Interhemispheric asymmetry of the ECoG sleep patterns of dolphin no. 8. A: electrode localization in parieto-occipital cortex. B and C: prominent ECoG delta-waves in all three points of one hemisphere simultaneously with the ECoG desynchronization in all three points of the other hemisphere. The records C were obtained one hour later than those of B. Unipolar registration.
583
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~I S AM Fig. 2. Diagram of ECoG stages 1 (desynchronization), 2 (intermediate synchronization) and 3 (maximal synchronization)in left (L) and right (R) hemispheres during two differentnights (A and B) in dolphin no. 9. Bipolar recording from roughly symmetricalareas of the parietal cortex. Time scale in hours. The beginningof diagram A corresponds to the end of feeding; that of diagram B to the end of a 60-h period of total sleep deprivation.
Up to now, stage 3 has only been observed unilaterally. However, bilateral deltawaves of maximal amplitude have been observed during barbiturate narcotization, but only after autonomic respiration stopped. Interhemispheric asymmetry was observed in 6 of 9 investigated animals. In the first three experimental animals this asymmetry was not observed, but this is believed to be because only limited bilateral ECoG records were made with these animals. The male no. 9 had the following total time percentage of sleep-wakefulness stages during a 72-h session: bilateral desynchronization occupied 56.8 ~ ; bilateral synchronization (stages 2 and 2, or 2 and 3) occupied 0.8 ~ ; unilateral synchronization occupied 42.4 ~ of recording time, of which right-side synchronization occupied 14.7 ~ (stage 2, 9.6 ~ and stage 3, 5.1 ~) and left-side synchronization 27.7 ~o (stage 2, 19.1 ~ and stage 3, 8.6 ~o). No behavioural differences were found in our experimental conditions between states characterized by bilateral ECoG synchronization and by unilateral synchronization. The animals were practically immobile in both states. Apart from respiratory movements, the only other small movements visible were of the the fins and fluke, for postural maintenance. During the periods when one eye was open and the other was closed 1 the ECoG synchronization as well as desynchronization might be observed in either hemisphereL It is concluded that the unilaterally synchronized hemisphere is in SS, because the synchronized pattern of the dolphin is so typical of slow-wave activity of all mammals. The unilaterally desynchronized hemisphere is most probably awake. It cannot, however, be excluded that the unilaterally desynchronized hemisphere is in PS, since this phase of sleep is also characterized by ECoG desynchronization, and typical PS has not yet been found in the dolphin. The functional significance of the alternating interhemispheric asymmetry is still unclear. Of possible explanations, the performance of sentinel functions by the unilaterally desynchronized hemisphere, or the impossibility of maintaining respira-
584 tion d u r i n g bilateral delta-sleep, or during bilateral PS, are speculative. The n e u r o p h y siological m e c h a n i s m o f the observed p h e n o m e n o n is also unclear. It is hypothesized t h a t different levels o f activation in the two hemispheres result f r o m functional independence o f the two halves o f some activating or deactivating system in the b r a i n stem.
1 Lilly, J. C., Animal in aquatic environments: adaptation of mammals to the ocean. In D. B. Dill (Ed.), Handbook of Physiology--Environment, John Wiley and Sons, New York, 1964, pp. 741-747. 2 Mukhametov, L. M. and Supin, A. Y., EEG study of different behavioral states in free-moving dolphin (Tursiops truncatus), J. high. nerv. Activ., 25 (1975) 396-401 (in Russian). 3 Serafetinides, E. A., Shurley, J. T. and Brooks, R. E., Electroencephalogram of the pilot whale, Globicephala scammoni, in wakefulness and sleep: lateralization aspects, Int. J. Psychobiol., 2 (1971-1972) 129-135. 4 Shurley, J. T., Serafetinides, E. A., Brooks, R. E., Eisner, R. and Kenney, D. W., Sleep in cetaceans. I. The pilot whale, Globicephala scammoni, Psychophysiology, 6 (1969) 230.
