Unihemispheric sleep deprivation in bottlenose dolphins

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1 .. Sleep Res. (1992) 1, Unihemispheric sleep deprivtion in bottlenose dolphins A.. OLEKSENKO, L. M. MUKHAMETOV,. G. POLYAKOVA, A. Y. SUPN nd V. M. KOVALZON Severtsov nstitute of Evolutionry Morphology nd Ecology of Animls, Acdemy of Sciences, Moscow, Russi Accepted in revised form 11 December 1991; received 30 October 1991 SUMMARY Unihemispheric nd bihemispheric sleep deprivtion were performed in bottlenose dolphins. One brin hemisphere ws cpble of being deprived of delt ( Hz) sleep in the former condition. Here, n increse in sleep pressure ws observed during sleep deprivtion in the deprived hemisphere. n the recovery sleep, following unihemispheric sleep deprivtion, there ws rebound of delt sleep only in the deprived hemisphere. Following bihemispheric sleep deprivtion the nimls exhibited n increse in delt sleep in both hemispheres. KEYWORDS bottlenose dolphins, delt sleep, interhemispheric reltions, sleep deprivtion, unihemispheric sleep NTRODUCTON To dte, the ppernce of slow wve sleep in one hemisphere t time ( unihemispheric slow wve sleep) hs been recorded in representtives of ll three orders of qutic mmmls: Cetce, Sireni nd Pinnipedi (Serfetinides et ul. 1972, Mukhmetov nd Supin 1975; Mukhmetov et l. 1977, 1985, 1988, 1990; Mukhmetov 1984, 1985, 1987, 1990). This form of sleep is most pronounced in dolphins. They mnifest no bilterl delt synchroniztion (lrge mplitude slow wves) in the EEG, nd show reltively little bilterl intermedite synchroniztion (slow wves with smller mplitude thn delt wves, see below). No prdoxicl sleep hs been identified in dolphins (Mukhmetov 1988). n summry, their sleep predominntly consists of unihemispheric slow wve sleep. This unique sleep structure in dolphins llows experiments to be performed which re not possible in other mmmls. Our preliminry studies indicte tht it is fesible to deprive one brin hemisphere of slow wve sleep while sleep continues in the other hemisphere (Mukhmetov 1984). To dte, we hve been ble to do this in severl bottlenose dolphins. To our knowledge, sleep deprivtion (SD) studies in other mmmls hve involved the entire brin. The present study summrizes the results of unilterl nd bilterl SD experiments in bottlenose dolphins obtined Correspondence: L. M. Mukhmetov. Severtsov nstitute of Evolutionry Morphology nd Ecology of Animls, USSR Acdemy of Sciences, Leninsky prospect, 33, Moscow, , Russi. over mny yers. n prticulr, we ddressed the following issues. (1) The fesibility of performing unihemispheric SD while sleep continues in the other hemisphere. (2) Whether there re ny indictions of n incresed sleep pressure during the course of deprivtion. (3) Whether unihemispheric sleep rebound occurs fter discontinution of the unihemispheric SD. METHODS The study ws performed with seven, dult, Blck Se bottlenose dolphins (Tursiops run ct us), weighing kg, nd cm long. Bihemispheric SD experiments (n =6) were performed on six nimls nd unihemispheric SD experiments (n = 9) on five nimls (Tble 1). Electrodes were implnted in nimls under locl nesthesi (2% novocin solution) on pproximtely symmetricl res of the prietl cortex, for bipolr nd unipolr recordings of the electrocorticogrm (ECoG) of the two hemispheres (for detils see Supin nd Mukhmetov 1986). During the experiments the dolphins were exposed to nturl photoperiod while they could swim freely in n open-ir tnk (5 x 5 x 1.2m) to which they were welldpted. The durtion of dpttion time ws 2-8 weeks. Artefct-free cbles nd slip-ring connector were used to connect the electrodes with the polygrph input. Continuous polygrphic recordings (pper speed 7.5 nd 15 mm s-) 40

2 ~ ~~~~~ ~ ~ Unihemispheric sleep deprivtion 41 Tble 1. Told time of sleep stges (% of totl recording time)** Number Durution Durution of of of the SD the recovery Buseline period SD period experi- period period ments ' Sex (h) (11) Stuge 2 Stuge 3 ~ ~ ~~ Deprivtion of right hemisphere 78-1 Mle 82-3 Femle 83-1 Femle 84- Mle 84-lb Mle 85-2 Femle f ~ f f f 0.10 Deprivtion of left hemisphere 83-1 Femle 84-l Mle 84-lb Mle f f f f 0.15 Deprivtion of both hemispheres 15-2 Mle 82-3 Femle 83-1 Femle 84-1 Mle 85-1 Femle 85-2 Femle * f f f 0.05 ~ * The numbers represent the yer of the experiment (75-85: ), the number of dolphins during tht yer (, 2.3) nd the number of SD experiments on the sme niml (, b). ** The totl sleep stge times, seprtely for stges 2 nd 3, occurring in the deprived hemisphere during the unihemispheric SD period or in both hemispheres during the bihemisphcric SD period f = Stndrd devition were obtined during prolonged sessions lsting up to 3 weeks. Vigilnce sttes were determined for 30-s epochs on the bsis of the ECoG. Three stges were identified. Stge 1. ECoG desynchroniztion. Srge 2. ntermedite synchroniztion including sleep spindles, with slow wves in the thet nd delt rnge, the mplitude of which exceeded the verge mplitude of the wves of Stge 1 by greter thn fctor of 1.5. The slow wve episode ws longer thn 10 s, nd the totl durtion of the delt wves of the mximum mplitude ws less thn 50% of the 30-s scoring epoch. Stge 3. Delt synchroniztion in which the totl durtion of Hz slow wves of the mximum mplitude exceeded 50% of the 30-s scoring epoch. The ctul voltges of EEG wves in these experiments is problemtic s this depends strongly on the chrcteristics of the individul electrodes nd on the loction of the electrode tips with regrd to the cortex (epidurl, intrcorticl etc). The sleep behviour of these nimls is indistinguishble from tht of quiet wkefulness; there is stereotyped quiet swimming in circle. Sleep deprivtion ws performed either by rousing the nimls by slps on the wter surfce or by wek electroskin stimultion of the flipper. There were no differences in the responses to these two deprivtion methods. Usully, ECoG slow wves ppered in one hemisphere only. During the unihemispheric SD the nimls were stimulted if the intermedite ECoG synchroniztion ppered on the polygrph for 10-15s in the hemisphere tht ws being subjected to SD. Stimultion ws continued until the ECoG remined desynchronized in the deprived hemisphere. ECoG slow wves ppering in the non-deprived hemisphere were not interrupted. Occsionlly both hemispheres went to sleep simultneously. Such sleep episodes were lso interrupted during unihemispheric SD, which lso necessitted disturbing the nturl sleep development in the hemisphere which ws not being subjected to SD. During the bihemispheric SD the dolphins were stimulted if the intermedite ECoG synchroniztion ppered in either of the two hemispheres. Recordings included -h bseline session followed by severl dys of SD, nd one -h recovery dy. n four experiments out of the 15 the recovery period ws shorter thn h. n such experiments the corresponding period of dy nd night of the bseline session ws used for comprison, s it hd been demonstrted erlier (Muk-

3 42 A. 1. Oleksenko et 1 hmetov et l. 1988) tht bottlenose dolphins exhibit mrked circdin rhythm of sleep. The durtion of the deprivtion period ws vried individully becuse ech niml rected differently to SD. Thus, the bihemispheric SD lsted from 1.5 to 3 dys, nd the unihemispheric SD from 2 to 6 dys (Tble 1). The SD ended t vrious times during the -h period in different experiments. RESULTS The SD induced n lmost complete loss of Stge 3 in one or both hemispheres, depending on the deprivtion type (Tble 1 nd Fig. 1). During the course of both bihemispheric nd unihemispheric SD, the occurrence of Stge 2 ws firly substntil, nd in six cses exceeded bseline vlues. This ws the result of greter ttempts by the nimls to go to sleep. The increse in sleep pressure during the course of SD ws determined by computing the number of induced wkenings every h. The generl number of wkenings required for the deprived hemisphere during the lst dy of unihemispheric SD ws higher thn tht for the first dy of SD in ll nine experiments (Fig. 2). The difference ws significnt ccording to the Wilcoxon-test (P < 0.01). n ll six bihemispheric SD experiments, totl sleep time (Stge 2 nd 3), or the mount of totl delt sleep (Stge 3) in both hemispheres, ws higher fter deprivtion compred with the bseline (Fig. 3b). The totl delt sleep time (see Fig. 1) for single hemisphere fter bihemispheric deprivtion ws in most cses higher thn the levels before deprivtion (Fig. 3b). After unihemispheric SD, delt sleep in the deprived hemisphere (either right or left) invribly exceeded the bseline vlues for the sme hemisphere (Fig. 3). During recovery from SD, delt sleep in the non-deprived (A) b # d d d3 d5 Figure 1. Vigilnce sttes in the two hemispheres (L: left hemisphere; R: right hemisphere) in n individul bottlenose dolphin (N 85-2) during bseline (b), during severl dys of unihemispheric (A) or bihemispheric (B) sleep deprivtion (dl-d5), nd the recovery dy (r). The rrows indicte the beginning nd the end of the sleep deprivtion period. The vigilnce sttes, bsed on the ECoG pttern, re: 1. desynchronized; 2. intermedite synchroniztion nd 3. delt synchroniztion (see Method, nd the insert t the top of the figure). The time of dy is given t the bottom. r Time of dy (h)

4 Unihemispheric sleep deprivtion (A) bl 9 z d N & 300- U 01._ l c r r 0 l n 5 z b b Figure 2. Stimultions during unihemispheric SD. The left columns of ech pir represent the number of wkenings per h on the first dy nd the right columns the lst dy of SD. The numbers tht identify SD experiments under the columns re the sme s those in Tble 1. The first three pirs of columns A correspond to the experiments with the left-side SD nd the next six pirs B-to experiments with right-side SD. 5m1 (A) L (B) n " Figure 3. The occurrence of delt sleep for the individul nimls during recovery from sleep deprivtion (A: unihemispheric SD, nine experiments; B: bihemispheric SD, six experiments) expressed s percentge of the bseline vlue (= 100%) in the corresponding hemisphere. The columns represent the vlues of the left hemisphere (left columns) nd the right hemisphere (right columns) seprtely. The blck columns indicte which hemisphere hd been subjected to SD (left = three experiments; right = six experiments). The numbers of SD experiments under the columns re the sme s those in Tble 1.

5 44 A. 1. Oleksenko et l. hemisphere could either be bove or below its bseline vlue. There were cler individul differences in ll these rebound effects but t present the resons for this re uncler. The totl delt sleep time in the deprived hemispheres ws usully higher t the beginning of the recovery period nd then decresed. This decrese intercted with the circdin rhythmicity of sleep. Quntittive nlysis of the sleep EEG ws not performed. During the norml sleep of bottlenose dolphins there is tendency for sleep epochs to lternte from hemisphere to hemisphere. After termintion of sleep epoch in one hemisphere the probbilitv of initition of the next epoch in the second hemisphere is twice s high s the one for the sme hemisphere (Mukhmetov et l. 1988). During SD, this tendency to lternte between the hemispheres persists nd is mnifested in the lterntion of ttempts to initite sleep. During the recovery of both unihemispheric nd bihemispheric SD, the lterntion of sleep epochs between the hemispheres ws more pronounced thn during the bseline. Wheres during the bseline conditions 67% of sleep epochs were followed by sleep in the contrlterl hemisphere, fter bihemispheric SD the lterntion ws 87%, nd fter unihemispheric SD this ws 80%. The lterntion of sleep epochs ws prticulrly pronounced t the beginning of the recovery. DSCUSSON The present study demonstrtes tht it is fesible to perform unihemispheric SD in bottlenose dolphins. An incresed sleep pressure ws indicted by the incresed number of stimultions required to mintin wking ECoG pttern in the deprived hemisphere. Clerly, sleep pressure incresed both during bihemispheric nd unihemispheric SD. Furthermore, unihemispheric SD ws followed by unilterl rebound of delt sleep. These experiments re the first to demonstrte tht SD cn be ccomplished not in the whole brin, but in prt, i.e. in single brin hemisphere. This phenomenon, s well s the norml pttern of unilterl sleep in dolphins, indictes tht ech hemisphere is essentilly utonomous in the genertion of sleep. A diffuse, non-specific sleep regultion which encompsses simultneously both hemispheres is not obligtory in the dolphins. On the other hnd, the regulr lterntion of sleep between the hemispheres demonstrtes tht both hemispheres interct during the sleep process. The lterntion of sleep between the hemispheres indictes tht there is reciprocl interction between the hemispheres which regultes the sleep process. The bove evidence provides grounds for us to believe tht prt of the brin, in this cse one hemisphere, hs pronounced intrinsic need for sleep, which cnnot be compensted for by sleep occurring in the other hemisphere. ACKNOWLEDGEMENT The uthors would like to thnk Dr rene Tobler for her vluble help in editing this pper. REFERENCES Mukhmetov, L. M. Sleep in mrine mmmls. Exp. Brin Res., (SUPP. 8), 1984: Mukhmetov, L. M. Unihemispheric slow wve sleep in the brin of dolphins nd sels. n: S. noue nd A. A. Borbily (Eds) Engodeneous Sleep Substnces nd Sleep Regultion. Jpnese Scientific Societies Press, Tokyo, YNU Science Press BV, Utrecht, 1985: Mukhmetov, L. M. Unihemispheric slow-wve sleep in the Amzonin dolphin, ni geofrensis. Neurosci Lett. 1987, 79: Mukhmetov, L. M. The bsence of prdoxicl sleep in dolphins. n: W. P. Koell, F. Obl, H. Schulz nd P. Visser (Eds) Sleep 86. Gustv Fischer Verlg, Stuttgrt, 1988: Mukhmetov, L. Le sommeil des mmmiferes mrines. L Recherche, 1990, 21: Mukhmetov, L. M., Lymin, 0.., Chetyrbok,. S., Vssilyev, A. A. nd Dis, R. Sleep nd wkefulness in n Amzonin mntee. n: J. Morne (Ed.) Sleep YO. Pontengel Press, Bochum, 1990: Mukhmetov, L. M., Lymin, 0.. nd Polykov,. G. nterhemispheric synchrony of the sleep EEG in northern fur sels. Experienti, 1985, 41: Mukhmetov, L. M., Oleksenko, A.. nd Polykov,. G. Quntittive chrcteristic of the ECoG sleep stges in the bottlenose dolphins. Neurophysiology, 19%. 20: (in Russin). Mukhmetov, L. M. nd Supin, A. Y. EEG study of different behviorl sttes in free moving dolphins (Tursiops trunctus), J. High. Neru. Actiu 1975, 25: (in Russin). Mukhmetov, L. M., Supin, A. Y. nd Lymin, nterhemispheric symmetry of the EEG during sleep in mrine mmmls. n: T. Onini (Ed.) Neurobiology of the Sleepwkefulness Cycle. Motenierebe, Tbilisi, 1988: Mukhmetov, L. M., Supin, A. Y. nd Polykov,. G. nterhemispheric symmetry of the electroencephlogrphic sleep ptterns in dolphins. Brin Res. 1977, 134: Serfetinides, E. A., Shurley, J. T. nd Brooks, R. E., Electroencephlogrm of the pilot whle, Globicephl scmmoni, in wkefulness nd sleep: ltcrliztion spccts. n!. J. Psychobiol / 1972, 2: , Supin, A. Y. nd Mukhmetov, L. M. Some mechnisms of the unihemispheric slo& wve sleep in dolphins. n: V. E. Sokolov (Ed.) Electrophysiology of Sensory Systems in Mrine Mmmls. Nuk, Moscow, 1986: (in Russin).