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IMPLICATIONS for FUNCTION in MICROGRAVITY Introduction Journal of Vestibular Research. Vol. 8. No.1. pp. 81-94.1998 Copyright I!:I 1998 Elsevier Science Inc. Printed in the USA. All rights reserved 0957-4271/98 $19.00 + .00 ELSEVIER PIT S0957-4271(97)00055-4 Review SLEEP AND VESTIBULAR ADAPTATION: IMPLICATIONS FOR FUNCTION IN MICROGRAVITY J. Allan Hobson, Robert Stickgold, Edward F. Pace-Schott, and Kenneth R. Leslie Laboratory of Neurophysiology. Massachusetts Mental Health Center, Harvard Medical School, Boston, Massachusetts : : ,. "" .. 1>.. .. I. II ~ ,... "" ,... " - r' - .... .. ,... .. ... ,. .. ~ 'f''''' .. .... p .... - - • .. _.... • - _ E-mail: [email protected] o Abstract - Optimal human performance de­ Introduction pends upon integrated sensorimotor and cognitive functions, both of which are known to be exquis­ The functions of sleep remain unknown. The itely sensitive to loss of sleep. Under the micro­ compelling idea that sleep subserves neuronal gravity conditions of space flight, adaptation of plasticity was first clearly articulated by Giuseppe both sensorimotor (especially vestibular) and cog­ nitive functions (especially orientation) must occur Moruzzi (1). This hypothesis has been tested in quickly-and be maintained-despite any concur­ many ways, induding the systematic perturba­ rent disruptions of sleep that may be caused by tion of the vestibular system. The close interre­ microgravity itself, or by the uncomfortable sleep­ lationship between the vestibular nuclei and the ing conditions of the spacecraft. It is the three-way sleep inducing structures of the pontine brain interaction between sleep quality, general work ef­ stem has been extensively studied by Moruzzi's ficiency, and sensorimotor integration that is the colleagues, especially Ottavio Pompeiano (2). It subject of this paper and the focus of new work in is the purpose of this paper to discuss the con­ our laboratory. To record sleep under field condi­ fluence of these two lines of thought and re­ tions including microgravity, we utilize a novel search in a new program of work on human system called the Nightcap that we have developed sleep in space and to present the results of the and extensively tested on normal and sleep-disor­ dered subjects. Tu perturb the vestihular system firsl studies conducted within thi s paradigm. The hasic idea i ~ that til t' sudden expo:-.ure to in ground-based studies. Wt utilize a variet~ of ex­ perimental conditiom including optokineti( stim­ illi.:rogra\'it: condillon:- \)' ~f1aC t 'nig h: I ul1 e­ ulation and hoth minif~' ing an(' rl'v~rsin!! !!og~it' tionall : a e": 0uple< tile ve.,tiQul a; oto li thi c (}rgan paradigm.'- that haw been extensivei~ studied in recepwr:. and ellillinate:-. tOlli e un ci pl1a ~l, ami­ relation to plasticity of the vestibulo-oculur reflex. gravity postural 'I d,iustment:.. Thi;, cOlll pe b the Using these techniques we will test the hypothesis organism to reprugram the vestihular system ~ o that vestibular adaptation hoth provokes and is that it can work in an exclusivel) inertial mode. enhanced by REM sleep under both ground-based This monumental reorganization constitutes a and space conditions. In this paper we describe natural challenge to the plasticity of the brain. If preliminary results of some of our studies. © 1998 sleep-and especially REM sleep-is involved Elsevier Science Inc. in enhancing plasticity, it would be desirable to monitor changes of sleep in space. To this end, o Keywords-sleep; vestibular adaptation; we have designed the Nightcap, a simple, porta­ REM sleep; microgravity. ble, and self applied measurement system which 81 82 J. A. Hohc;o!! p.1 al is compatible with the behavioral and opera­ may then both aILer and be altered by sleep tional constraints of space tlight (3). (since plasticity is both mediated and modulated In this paper, we review the rationale for se­ by the same neurones that are critical in deter­ lecting the vestibular adaptation model and the mining the absolute and relative amounts of evidence concerning its effects on sleep under NREM and REM sleep). normal gravity conditions. Then we show how The distinction between these two phases of the Nightcap could be used to assess the effects sleep is best appreciated by recognizing that on sleep of ~udden and prolonged exposure to during REM. the EEG and mutor pattern gener­ microgravity and cOl1lpare this approach to lhe ators of the upper brain are reactivateu to wak­ lradilional 1leep laboralllry methods thaI ha\ e ing levels. but motor l)L1tput is blocked by active heen ~ I..,ed until now in .lttel11pts to JncLlmcnt inhibition l)f all motorneLlrone~ eXL"ept those ·,"!licn n1l.l\ e the eye~, T,i.., ·in'mi· , 11~ I!Jnroach :~ in an ~arly :-,ta~e The rhree main phenomena or interest in thi~ uf Je\ el OlJl11elH. Tn ;noicute ;l\)W useful it may paper and the .pairwi:-ie links between them dt"l' be. ve ,Jresenl ..,ome prelil11inary dara from a illustrated :n Figure ~. We will argue that [here ground-based experiment in which subjects i~ a strong tie between the vestibuiar system and slept after exposure to optokinetic stimulation sleep on the one hand and between sleep and in a rotating drum. Its description here is of­ performance on the other. fered in the spirit of Giuseppe Moruzzi' s vision­ ary approach to the study of sleep function. The Vestibular System and iVIicrogravity When he first proposed his plasticity hypothe­ sis, he could not have dreamed that it might soon be tested in human beings hurtling through It is obvious that all normal sensorimotor in­ space. tegration depends upon the vestibular system. Whenever the head moves, the eyes must be ap­ propriately repositioned to maintain fixation on a target or to fixate on a new one. This vestib­ A Conceptual Framework ulo-ocular reflex (VOR) was first described by Lorente de No (4) and has been extensively In the ultimate paradigm of our interest, a studied (5). One robust feature of the VOR is its human being is exposed to the microgravity plasticity (6). When subjects are exposed to conditions of space. This immediately provokes novel conditions (for example. microgravity or vestibular reprogramming, a process which may distortions of visual input), the VOR must be affect both sleep (via changes in the excitability recalibrated. This adaptation can take hours or of control neurones) and ho- and is learned with variable speed by dif- learning that is essential to adaptation to space experimental measurement via a target acquisi- The Vestibular I -.......;~ Sleep and Psychomotor System and Sleep Performance ~.r---------J' f ~ The Vestibular System ~ and Microgravity Figure 1. The three main phenomena of interest in this paper and the pairwise links between them. Sleep and Vestibular Adaptation 83 tion task is a potent paradigm for measuring ad­ experience with sleep, the network is signifi­ aptation to rnicrogravity. cantly state-dependent: its sensitivity, gain, and It is not surprising that astronauts commonly operating properties change with changes in experience dysfunctional states upon exposure central state. A commonplace example is the re­ to microgravity and require extensive training lief of motion sickness by drowsiness and sleep. and variable periods of adaptation to acquire Indeed sleep is so often experienced as a re­ comfort and psychomotor competence in micro­ sponse to motion sickness as to suggest that it gravity. Motion sickness, nausea, and malaise may be an integral part of adaptation to sudden commonly hinder performance during the early changes in gravitational vectors. days of space flights, even in carefully selected The state dependent changes in the integra­ and highly trained subjects. It is typical for as­ tive network of the brainstem are regulated by tronauts to treat these symptoms with prometh- three well-known processes. One is simple dis- level falls during drowsiness and at sleep onset. occurred, astronauts may experience disorienta­ The second is aminergic demodulation. which tion of an explicit type (for example, unwit­ is a consequence of the decrease in noradrener­ tingly viewing an instrument panel upside­ gic and serotonergic input that begins at sleep down resulting in left-right confusion). For this onset and becomes most pronounced in REM. reason, major portions of the physiological re­ Aminergic demodulation also influences sensi­ search effort of the manned space flight pro­ tivity and gain, but has been further postulated gram have been appropriately dedicated to un­ to mediate sensitization, habituation, and other derstanding and countering these effects. We plasticity phenomena. The third, and by far the intend to link our studies to this knowledge base most interesting process, is the cholinergic demod­ and to build upon it. ulation of sleep onset and the subsequent cholin­ ergic hypermodulation of the network in REM. The net result of the concomitant aminergic The Vestibular System and Sleep demodulation and cholinergic hypermodulation is that the vestibular system operates off-line in Located in the pontine brainstem, the vestib­ REM sleep (8). In other words, REM sleep ular nuclei are adjacent to and integral with the changes the operating properties of the vestibu­ reticular neuronal machinery that controls the lar reflex network such that it performs internal human sleep-wake cycle (2,4,7). The vestibular operations upon self-generated signals without nuclei receive inputs encoding head position the perturbation or benefit of inputs and out­ from the vestibular end organ in tilt" labyrinth, put~. Ii i~ thi!o> chemically nltered autoacti\:ation and the~ integrate them with sip:nal'. encoding of the brain'~ proceci ural na vigati on network limb and trunk position 1'r01il peripheral pro- . thaI ha~ led man~ sleep researcher., to propose prioceptor!> in the lil11b~ and trun!.. :h~' \'e~l!h~,· . t!"!~l' f:2h( '-.1 r:.e;- ~·C' .. t:-·· ~ "' · ·I.I:.:":..·-J~!:.·~:~ . l~ : ~:· : ; i: ~ ~ ~ ~ lar neurones are also reciprocally innervated by theor) of specific relevance to human adapta­ the oculomotor neurons (cranial nerves III.
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