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
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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. IV. tion to microgravi lY. An i-'(ll11 orpilic thcory ha:-. VI) and the pontine reticular prt'-motor neUrons, been advanced with respect to the plasticity in These in turn control them ancl initiate appropri the hippocampal system that underlies learning ate postural adjustments when reflex conditions of spatial orientation in the explicit or territorial or task demands change (see the schematic sense. (For a review of such functional theories model in Figure 2). Other chapters in this vol of sleep, see reference 9.) ume document the link between the vestibular Two specific predictions can be made on the nuclei and the autonomic nervous system. basis of what is now known: (1) REM sleep will This massive brain-stem integrative network be enhanced as a direct response to microgravity, could be said to be the body's own navigational and (2) REM sleep will help to prCl111 i)te the ad- system. As we all know from nUl" f)\Vn \.:;eryday aptntir>:' ,11 pl:)<;" required to remoui.-i tht ::. , 84 J A. Hobson et al navigational network. We resist the temptation tation may be (in part) REM-sleep mediated and to digress here to a literature review of the many (2) that the REM sleep mediation of vestibular bases of this hypothesis and simply point out plasticity may be (in part) cholinergically mod that (I) many new learning challenges entail in ulated. It thus follows that pharmacological or creases in REM and are impaired by REM dep behavioral interventions that enhance REM rivation, and (2) new learning challenges that sleep might enhance vestibular adaptation. In involve vestibular adaptation may be particu deed, it is our umlerstanding that the anticholin larly REiVI-:.leep ~vocative and REM-sleep loss ergic agent scopolamine (which would be ex o;ensiti\~. As We indicate belO\v. it is ilOW feasi pected to block REM) has not proven useful in ble [() track veslibular adaptation ~llld sleep in helping humans adapt ro "pace. To the best of nanlkl Ilnde" :he 1)rolnn~ed Illicro~ravity con nur knowledge. [he REM sleep-vestibular ad Jilion~. .Iptation iink [har we propo~e to study has not A t'inal )n inr clOSeS [his section. ~E:VI sleep ./~t been made explicit in ~pace physiology and ,:an be illl Illediatdy triggered (in the short term) medicine. We hope to correct this oversight by by choiinergic l11icrostimuiatiol1 of ~he pontine testing ~everal novel and important hypotheses. reticular formation. In addition, the threshold for REM sleep can be lowered (in the long term) by cholinergic microstimulation of the caudal Sleep and Psychomotor Peiformance peribrachial complex in immediate proximity to the veSlibular complex (see Figure 2). These As anyone who has ever experienced a night findings indicate (1) that acute vestibular adap- of impaired sleep knows, the ability to attend to,
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VI
Figure 2. Schematic horizontal section of pontine bralnstem showing some proprioceptive network elements and their modulators. The vestibular nucleus neurons (V.N.) interact with reticular formation (R.F.) and oculo motor (VI) neurons to control the neurons 0 which mediate the vestibule-ocular reflex. This circuitry, Which Is depicted on the right-hand side of the schematic, receives three modulatory Inputs. that also mediate sleep ef fects: the serotonerglc raphe (5Hn, the noradrenergic locus coeruleus (NE), and the cholinergic peribrachlal nucleus (ACh). The short- and long-term REM sleep enhancement regions are shown on the left hand side of the diagram. Sleep and Vestibular Adaptation 85 process, and retain infonnation is adversely af rective ocular movement is under the control of fected by poor sleep. The literature on this sub the vestibular system and is known as the ves ject, pioneered by Wilkinson's group in the tibulo-ocular reflex (VOR). Under various con Human Performance Laboratory in Cambridge, ditions, these neuronal networks can learn to England, has been extensively confirmed by behave differently. One of the best studied para subsequent research (10). digms of vestibular learning involves the use of Recently a more exciting proposal has been distorting glasses (see reference 5 for a review). advanced: not only does sleep enhance perfor These glasses contain lenses that reverse left mance by preventing attentional lapses (a pro and right, reverse up and down, magnify or tective function), it actually serves to promote the "minify" (reduce to a smaller size) the retinal retention or consolidation of previously learned image of visual space. material (a conservative function). This second, In consultation with Dr. Jacob Bloomberg
fmdings ofKarni and Sagi (11,12). which indicate duce a scalar reduction in visual images so that. that new visual discriminative learning is retained with a two-fold reduction. an object that actu if and only if sleeping subjects enter REM. ally spans 20° of visual space will only span 10° If neocortically mediated visual learning also of retinal space. As a result, if a subject attempts proves to be REM sleep dependent, then the to move his gaze or turn his head toward a tar vestibular adaptation concept would have rele get that appears 10° to the left of a fixation vance not only to the space context but to plas point, he must actually move his eyes or head ticity enhancement in any context. Microgravity by 20°. Such tasks are referred to as "target ac might then be viewed as a particularly potent quisition" tasks (TATs) and involve the ballistic test of the hypothesis that vestibular-mediated movement of the eyes and head under the con plasticity alters (and is altered by) REM sleep. trol of the vestibular system. When minifying It is this concept that we will explore utilizing lenses are worn, the neural networks within the the Nightcap recording system. vestibular system adapt over a period of 2 to 4 hours, and subjects learn to make these move ments accurately while wearing the minifying Sleep, Dreams, and Vestibular Functions lenses. Both the time course of adaptation and the theoretical basis of this adaptation have One of the most remarkable features of been extensively studied. dreams is the ~ense of , weightlessness that ac Considerable research has also been carried companies oneiric flight , Thi~ unusual dre~lIi 'J ' out Llsing ,Dove pri~I11 ~ .. which prodUCt a kfi- tlll\. sensatIon., I~ so p Ieasura) II e t I1at ..Ii I~ 0 f'tGn soug III ri.uht_ re"ersal \,vith(lu! shih~ on the vertical by practitioners of lucid dreaming. Bu! i! has axi:-. . Wncn an llbjeci appe.arc. ir the lefi \ iSLlLli also prompted ~pecul.ati()li regardinf!i r~ nmsibk fiel o. the' ~ubj e~': mu s' actua!l: "hift hi ~ g~l:'e to physiological basis in the altered neurophysiol the rigillto brin~ the OL1.1ect Il! [i1t' loveal region. ogy of REM sleep. In this section. we discuss In this case. adaptation of the VOR lake~ con- data linking sleep and dreaming to vestibular siclerabl) longer, up [0 two weeks. and appears function. to be biphasic, with a relatively rapid (2 to 4-day) reduction in VOR gain and then a slower (6 to IO-day) adaptation of phase angle, leading first Sleep Responses to Vestibular Learning to diminished eye movement and then to a re with Distorting Glasses versal in direction of eye movement for a given head movement. When an individual turns his head, his eyes There are three lines of evidence that suggest automatically move in the opposite direction to that sleep may be affected by and, in turn, may "'d ! J '.lin ~tnbility of the visual field. This cor- affect this !en,.." 'g process. Fir" tllC' rlose J. A. Hobson at al
Pfl1,\: !Iity of the vestibular nllcleu!> to sleep cen Sh'C'i} and the Fictive M '-" '('lilCnf I lei:' in the pontine braiilslt.:Jll, the initiation of of DreL'1I II s eye movements during sleep, and the frequent occurrence of themes of movement and even Since formulating the Activation-Synthesis flight in dream reports all argue for the exist Hypothesis of Dreaming in 1977, our group has ence of functional interactions between these developed a set of quantitative probes that mea brain regions [(8,13,14,15), but see (17)]. Sec sure formal aspects of dream cognition, includ ond, some of the early studies of visual learning ing the illusion of movement. Our early work showed increases in REM sleep (16,18,19). Third. (22) showed that dreaming subjects perceived under conditions of sleep deprivation, subjects themselves to be constantly moving through the in our laborarory have reported that attempts at dream space. a finding that we have recently normal larget acquisition ~that is. without ;my contirmed amI extended (23). In this and other Jistorting lenses I resulted.: n pronounc~d under recenr 'york. we have shown [hal these dream ;1100[5 or thelr oadi!:>ric ,~yc movements. Taken featLlre~ ,lre RE iVI-sleep based and that this cor together. the ~ e provide 'I rationale for stud~/ing relation -.:an be J.decred with ~ he \Iightcap the relation~h i p , etween sleep. the visuo-oculo (23 .2-1- ). motor system. ,md [he \fOR under :lOrmal con One particularly interesting feature of ditions as well ~IS under conditions of modified dreamed movement (which we call "fictive" be vision (for example, minifying lenses), sleep cause it is illusory) is its "vestibular" content deprivation, and varied vestibular load (for ex (22). This feature is prominent in reports and in ample, microgravity). In this paper we focus volves sensations of noating, swimming, sail mainly on visuo-oculomotor effects. ing, flying, spinning, twitching, or turning, which dreamers generally regard as exciting or pleasurable. "Vestibular" dream content is in creased when subjects sleep in a swinging ham Sleep and Posture mock (25). To our knowledge, this dream fea ture has never been quantified and therefore In our early time-lapse photographic and never measured in subjects before and after ex video studies, we established the strong tempo posure to those shifts in vestibular input as oc ral correlation between major posture shifts and cur in microgravity. sleep stage transitions (20,21). This finding was As the vestibular system is initially per the foundation of our movement-based approach turbed by entry into microgravity, is the illusion to sleep stage detection now instantiated in the of dreamed movement changed? Can this Nightcap. Under normal gravity conditions, all change be tracked as adaptation occurs? What humans make, on average. two major posture new baselines are established under prolonged shifts per 90-minute sleep cycle: one tends to exposure? Finally, what is the sequence of
sess vestibular adaptation via its effects upon limb and head movements are observed (21). It the subjective experience of fictive movement is not known whether either the major posture in REM sleep dreaming. shifts or the head and the limb movements are gravity sensitive. Indirect evidence comes from astronaut reports of bizarre sleep postures in Measuring Sleep and space and of persistent limb elevations on Vigilance in the Field awakening from postt1ight sleep. Thus, gravity and micro gravity may exert differential effects This section will focus on two features of our upon sleep posture, and these may in tum affect Nightcap System of particular relevance to this the quality and quantity of sleep and even of paper: 1) its ability to reliably predict sleep dreaming. stages and 2) its ability to detect lapses of vigi- Sleep and Vestibular Adaptation 87
lance that occur at sleep onset and which may Nightcap is a wallet sized (10 cm X 7 cm X 2 interfere with performance during waking. Al cm) device weighing only 150 g and capable of though we focus mainly on sleep itself, it is im recording 10 nights' data on a single 9V alka portant to appreciate the potential of the ap line battery. Its internal memory can store data proach to detect the microsleeps that interrupt for up to 30 nights. waking. We therefore point out that work in Since both eyelid and head movements gen progress in our laboratory (26) shows clearly erate 10m V signals, they are easily detected that our eyelid sensor's output falls dramatically without electronic amplification. Furthermore, at sleep onset when EEG alpha synchrony is because the movements are digitized at the ac suppressed and hypnogogic reverie commences. quisition stage, they can be stored in Nightcap We believe that it is feasible and desirable to memory as events per minute. This eliminates
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.. - '." g .. e How Do Nightcap Data Compare 'with How Does the Nightcap Predict Polygraphically Recorded Sleep? Sleep Stage? We have now completed two studies com The history of the development of a 2-chan paring Nightcap measures with polygraphic nel state detection system is provided in previ (sleep lab) measures in normal and sleep-disor ous publications (21,30). The physical appear dered subjects (see Figure 4). Under conditions ance of the device is shown in Figure 3. The of gravity, there was an 87% agreement be-
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Figure 3. The Nightcap senses signals from a multipolar mercury switch on the head and a piezoelectric film on the eyelid and stores movement data in dynamic RAM. The data Is subsequently down-loaded to a Macintosh computer that identifies REM-nonREM-wake states according to a simple set of rules: 1) If there are counts in Lo'" channels it scores wake. 2) If there are counts in neither channel it scores NREM sleep '1 ' I' " re are eye lid counts but no head counts, it scores REM. A salr,ple record is shown in Figure 4 88 J. A. Hobson et al tween the Nightcap and the polygraph in the frequent in waking, drop precipitously at sleep scoring of l-min epochs (27,28,29). onset in conjunction with (1) the suppression of The head movement channel of the Nightcap alpha waves and (2) the subjective experience is roughly equivalent to the movement-artifact of hypnogogic mentation. The reason for this sensing function of the EMG, and movement time exquisite sensitivity is grounded in eyelid neu is thus a good index of the brief awakenings that rophysiology (see Figure 5). often interrupt sleep. Under microgravity condi The eyelid is raised by the levator palpebrae tions. we will determine if head movement is still (LP) muscle as indicated in Figure 5B. The eye a sen~i(i\'e or ,~elecrive index of such awakenings. liLi is controlleLi by brain stem neUl'ones thm The eve/it! sensor is a piezoelectric [jim ap project directly to the levator palpebrae muscle. ::.-1!ec! tl' '!~';! ~it~ ,!,:!~ ;c 'er.,iri"e 'tn 'lnc!er!;,ing The LP muscle j" thus monosynaptically inner eye movemenrs; ~he corneal bulge distorr!> the vated by u.;wnal branches of oculomotor neu lid every time the eye moves. Nightcap eyelid rons in the caudal central division of the oculo "ensor counts ':i1rrelate well with REMs identi I11ntnr nllc leLis (3 Il. It is probably for this tied by EOG (28). reason that the eyelid piezo film is us good a vigilance detector as it is a REM sleep detector! The result is that a single system raises the lid How Does the Nightcap Detect SLeep and the eye with each upward gaze, Like the ex Onset and i\lIicrosLeeps? trinsic ocular muscles, the LP muscle contains fast twitch fibers that mediate the coordinate An unexpected property of the eyelid move movements of eye and lid during upward gaze ment sensor is its exquisite sensitivity to sleep displacement. But the LP also contains slow onset and microsleeps. We have recently found twitch fibers of the sort found in skeletal anti (26,32) that eyelid movements, which are very gravity muscles that maintain posture (31), These
Eye Movements
Body Movements 12:00 1 :00 2:00 3:00 4:00 5:00
Figure 4. A typical night of sleep recorded simultaneously with nightcap and sleep lab polysomnography (sam ple output and analysis). Top trace: histogram of Nightcap-detected eye movements; second trace: hypnogram representing the manually scored polysomnograph record; third trace: hypnogram of computer-scored Night cap data; Fourth trace: histogram plotting Nightcap-detected body movements. On both hypnograms, the top level represents wake, the second (darkened) level represents REM, and the third level Is non REM. Periodic movements are not shown on the hypnograms. The lower axis Indicates the time of night. Sleep and Vestibular Adaptation 89 slow twitch fibers actively hold the lid open via put of the RF, as occurs at sleep onset and with tonic activation signals from the brainstem (31). attentional lapses, will be reflected in 1) an im It is known (as shown in Figure 2) that the mediate decrease in eyelid sensor counts, 2) pontine reticular fonnation neurons are premo EEG changes, and 3) cognitive and perfor tor controllers of the oculomotor nuclei (for ex mance decrements. ample. VI in Figure 2 and III in Figure 5B) and It is for these reasons that we see the eyelid hence of the LP muscle. It is this highly spe sensor as possibly useful in providing measures cific, fine-tuned system that the Nightcap eyelid of alertness as well as sleep. But we also note. sensor monitors. Naturally, any decrease in out- in passing, the possible value of the eyelid sen- A
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Figure 5. Schematic sagittal section of head showing position of nightcap head and eyelid sensors. (A) Note that head movement is integrated with eye position (and posture, not shown) by means of head position signals arising in the labyrinth impinging on the vestibular neurons Vlll and transmitted to neck muscles (XI). (8) Note that the eyelid is innervated by fibers from the oculomotor neurons (lll), which also Innervate the superior rec tus muscle. For comparison to the circuitry for Figure 2, the relative positions of the abduceus nucleus and nerve (Vi) are also shown. 90 J. A. 1- . )bson at al sor in vestibulo-ocular retlex monitoring. Many On retiring before sleep, the subject puts on scientists now measure this function using D.C. the bandanna and sensors, and then turns the electro-oculography, whose output could be Nightcap recorder on. A flashing light signals if compared with our eyelid sensor in collabora the battery needs to be replaced. On waking, the tive studies with a view to developing a multi subject shuts off the recorder and removes the purpose headgear system. Nightcap headgear. The time, effort, and dis comfort involved are minimal, another major advantage over standard recording techniques. HoyV' Is the Nightcap System, ActuuLlv Used? Sleep in Space in .lddition to lhe ~)hys;c:IJ ~CDnoml~~ al !'eady enumerated. [he N ightca!) (Figure 3) is ..-\Ithough sieep is nnrorioLlsly fugitive in ex extremely user-frienLily. In its ..:urre11l configu treme conditIons such :l~ high altitudes. it hus r:ltion. subjects simply tie a bandanna kerchief been Jifficult :0 obt:.tin satisfactory Jata from around their healh before retiring. The head humans exposed to microgravity. Standard re movement sensor is sewn into the bandanna and cording techniques require time-consuming is self-positioning when the subject aligns the electrode attachment, are themselves sleep in previously attached eye sensor with the center hibiting, and involve complex analog signal of the left eye. A plastic film is peeled away from processing. In this section, we provide an over the sensor, and it is self-applied to the left eyelid view of the published data. to which it adheres fmnly overnight. The eye Table 1 summarizes many of the sleep stud sensor is removed in the morning and discarded. ies performed to date in space. Reviews of sleep
Table 1. Selected Studies on Sleep In Space with and without Polysomnography
First # space In-flight # Days N Pre-flight sleep sleep Subjective for and sleep epoch epoch Post-flight sleep Reference Mission mission species' PSGt PSGt PSGt PSGt PSGt assessment
Gemini 7 7 1 hu EE + + 2
Quadens and Spacelab 1 18 + + 2 + Green (43) Gazenko Vostok, 1-5 5 hu EE, EO j: (41) Voskhod Gundel et al ? 8 1 hu + + 5 + (37) Santy et al Space Shuttle 7 58 hu 0 + (34) Shlyk et al Cosmos1667 7 2 rh +7 7 7 7 ;- (39) Stoilova et al Mir 7 7 hu +? 7 7 7 7 ? (45)§
• Species coded as follows: hu = human, ma = macaque (Maeaea nemestrina), rh = rhesus monkey. tNumber or "+" refers to polysomnography (PSG) studies (EEG, EOG, and EMG) reported to have taken place. When only cer- tain channels specified, EE = EEG, EO = EOG, EM = EMG. *Sleep and wake states not differentiated in reports on EEG and EOG findings. §Cited In Gundel et al. (37). Sleep and Vestibular Adaptation 91
in space among Apollo (33) and Space Shuttle decrement compared to pre-flight baselines as (34) astronauts have documented frequent sub measured by sleep latency, total sleep time, jective sleep difficulty and use of sleep medica number of awakenings, or subjective reports. tion, but do not report any polysomnographic The subject studied on the 84-day mission expe data. Lack of EOG prevented unequivocal mea rienced sleep difficulties during the first half of surement of REM in early EEG studies on the his flight, while the occasional insomnia re Gemini 7 astronaut (35.36). A recent polysom ported by all 3 men wa& attributed to work nographic study of space sleep in one subject schedules rather than to microgravity effects. (37) documented circadian shifting, redistribu Among U.S. studies, only Quadens and Green tion of slow wave sleep, shortened REM la (43) report any PSG data with EOG for the first tency, and decreased REM during the second sleep period in space. These authors were able REM-NREM cycle but, again, did not record to record EMG and EOG in a single Spacelab 1 first two
out the missions (38.39). In addition, EOG re matic increases in 1) REM percent, 2) eye move cording of the Biosatellite III monkey revealed ments, and 3) the relative occurrence of fast eye movement abnormalities in the early part of (> lis) versus slow (0.5 to 1.0/s) eye movements J the flight (40), and similar phenomena may oc during the first sleep epoch in space (3 h) when cur in humans (41). compared to either the second sleep epoch in Among U.S. studies, only Frost and col space (6 h), pre-flight baseline nights, or post leagues (42) recorded a large number of poly flight recovery nights. By the second sleep ep p somnograph (PSG) nights in space on replicate och in space, these sleep parameters (as well as subjects. In three Skylab missions lasting 28, sleep duration) had returned to baseline levels. 59, and 84 days, this group monitored sleep On the second day after return to earth, the ele EEG during pre-flight (3 nights), in-flight (12 to vation in relative occurrence of fast versus slow 20 nights), and postflight (3 nights) periods in eye movements (but not in overall eye move one crew member per mission. Again, no in ment frequency) recurred. These authors inter flight recordings were made on the first two pret these eye movement elevations as reflecting nights in space. the learning and integration of new information nt The only change in REM sleep consistently related to the return to normal gravity. found over all three missions was an increase in REM time and a decrease in REM latency which occurred late in the posr~f7ighr period (42). Optokinetic Stimulation and Sleepiness In-f1ight average REM percent wa~ either slightly
lower (especiall) late in the missions J 0:' un A:-. L first step in OUi' enort~ to establish a changed as compared to pre-nigh! baseline:, causal iink between \ ' ISUO- ,.:uloillowr stimula Since the post-flight REf\f. elevation occurreci lion anci sleep. we exposec human <;ubjects to late in the post-flight perioci and wa~ sustained optokinetic stimulation t Uh.~) en sul'l~CleI1l over more than one night. these authors hypoth strength to cause both subjective drowsiness esized that it wa~ nor a rebound effect due to and 'nausea and then measured tht' time taken to pre\ ious REM deprivation but, rather, wa~ a re fall asleep immediately thereafter and on the sult of re-adaptation to normal gravity. They nights following stimulation. Measures were pointed out that REM effects during adaptation derived from Nightcap parameters in both the to micro gravity may have been missed since sleep latency tests (MSLT) and the home-based sleep during the first 3 nights in space was not nocturnal sleep assessments-and are reported recorded. Other sleep changes observed on all in full elsewhere (44). ;er- three missions were an increase in stage 3 dur To produce optokinetic stimulation of the ing flight and a decrease in stage 4 post-flight. vestibular system, we placed the subjects in a Sleep quality did I thetic nervous system (for example, sweating), National Institutes of Health (MH 13,923 which probably worked against the soporific -1-8 .832) and the Mind-Body Network of the Mac drive of the vestibular stimulation. On this Arthur Foundation. REFERENCES l. Moruzzi G. The functional significance of sleep with 4. Lorente de No R. Vestibulo-ocular reflex arc. 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