Chapter 7 the Phylogeny of Sleep
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Handbook of Clinical Neurology, Vol. 98 (3rd series) Sleep Disorders, Part 1 P. Montagna and S. Chokroverty, Editors # 2011 Elsevier B.V. All rights reserved Chapter 7 The phylogeny of sleep KRISTYNA M. HARTSE * Sonno Sleep Center, El Paso, TX, USA INTRODUCTION the extent to which definitive statements can be made about the origin of sleep. However, by studying living, Why do we sleep? Despite a voluminous body of scien- phylogenetically ancient organisms such as insects, tific and clinical literature, the definitive answer to this fish, amphibians, reptiles, and primitive mammals, fundamental question has yet to be found. To the clues to the function of sleep might be revealed. insomnia patient with unrelenting chronic sleepless- This phylogenetic approach to investigating the ori- ness, the answer is painfully and viscerally obvious. gins of sleep has not been without controversy, and Sleep prevents feelings of sleepiness and dysphoria there is disagreement in the literature about the pres- during the day. To the scientist and clinician, however, ence or absence of sleep in nonmammals. There is gen- this answer, although responsive to the universally eral agreement that most nonmammalian organisms acknowledged effects of sleep loss, does not address exhibit behavioral sleep or rest. However, the electro- the specific biological or functional reasons for sleep physiological signs of sleep in nonmammalian organ- (Rechtschaffen, 1998). isms may be very different from that of mammals. All mammals and birds studied to date exhibit This observation has led some authors to conclude that, unambiguous signs of sleep. Furthermore, an array of by definition, nonmammalian species do not sleep specific human sleep disorders, including sleep apnea, because mammalian electrophysiological correlates of narcolepsy, periodic limb movements, restless legs, sleep are not present (Walker and Berger, 1973). These and insomnia, correlate with deficits in health and issues will be reviewed as we examine evidence for the well-being. These consequences of disturbed sleep in origins of sleep. conjunction with the universality of sleep in mamma- lian organisms imply that sleep serves an important THE DEFINITION OF SLEEP life-enhancing or even life-sustaining function. Corre- lations, however, do not prove causality. Whether the Sleep is defined by both behavioral and electrophysio- function of sleep can be discovered by studying human logical criteria. The well-established behavioral criteria sleep disorders or more generally by studying neuro- include: (1) a species-specific posture; (2) behavioral logically and biochemically complex mammalian spe- quiescence; (3) elevated arousal thresholds; and (4) cies is questionable. rapid state reversibility with moderately intense stimu- A different approach to discovering the origins and lation to distinguish sleep from hypothermia, torpor, or functions of sleep would be through the study of non- coma (Flanigan et al., 1974). Sleep homeostasis, the mammalian organisms which have remained relatively compensatory rebound in sleep after deprivation of unchanged from their ancient fossil ancestors and quiescent states, is an additional feature in the defini- which may provide clues about the origins of sleep. tion of sleep (Tobler, 2005). In mammals and birds, The presence of behavioral and electrophysiological there are distinctive electrophysiological correlates that signs of sleep in living mammals and birds suggests accompany behavioral sleep. As a result of the close that sleep has been perpetuated in evolution from relationship between behavior and electrophysiology, ancient origins. A behavior such as sleep, of course, electrophysiological correlates are almost universally does not leave a fossil record, which severely limits substituted for behavioral observation to define the *Correspondence to: Kristyna M. Hartse, Ph.D., Clinical Director, Sonno Sleep Center, 1400 George Dieter, Suite 210, El Paso TX 79936, USA. Tel: 915-533-8499, E-mail: [email protected] 98 K.M. HARTSE presence of sleep. Slow-wave sleep (SWS) is marked by findings have suggested that the spikes are a nonmam- high-amplitude neocortical slow waves. Cyclically alter- malian electrophysiological correlate of SWS. Persua- nating with SWS is rapid eye movement (REM) sleep sive evidence for REM sleep in nonmammalian (also called paradoxical sleep), characterized by low- organisms is not strong. Because the appearance of the voltage brain activity similar to that of waking, skeletal reptilian spike is substantially different from the neocor- muscle inhibition, and REMs. Although the distribu- tical slow waves recorded in mammals (Figure 7.1), tion and amounts of non-REM (NREM) and REM these findings have led some investigators to conclude sleep vary widely among mammals and birds (Zeplin that the spike is not an electrophysiological marker of et al., 2005), the electrophysiology of these two states sleep (Walker and Berger, 1973). Further studies in the is well established except in cetaceans (whales and rat and cat, however, have revealed the presence of a dolphins) and a monotreme, the echidna, a primitive spike recorded from the ventral hippocampus (VH) dur- egg-laying mammal (Mukhametov, 1987; Siegel et al., ing SWS which is similar to the reptilian spikes (Metz 1996; Lyamin et al., 2002, 2004, 2005). and Rechtschaffen, 1976; Hartse et al., 1979). VH spikes The electrophysiological correlates associated with and reptilian spikes have a similar morphology: they both nonmammalian behavioral sleep have received consid- show a rebound following enforced wakefulness, erable attention. No change in brain activity during and they both respond similarly to pharmacological behavioral quiescence, slow waves during waking agents. Additional support for a relationship between which diminish with behavioral sleep, both the presence hippocampal spikes and neocortical slow waves is the and absence of SWS, and both the presence and finding that hippocampal sharp waves are modulated absence of REM sleep have all been reported. How- by neocortical activity during SWS (Sirota et al., 2003). ever, some of the most rigorous studies, particularly The generation of slow waves requires neocortical in reptiles, have revealed the presence of a high-voltage development, and slow-wave activity recorded from spike which is prominent during behavioral sleep brain surface electrodes is easily observed in mammals and minimally present during behavioral wakefulness that have extensive neocortical development. However, (Flanigan, 1973, 1974; Flanigan et al., 1973, 1974). The the rudimentary neocortex of fish, amphibians, and spikes increase in a homeostatic response following reptiles in comparison to mammals would seem to pre- enforced wakefulness, and both spikes in reptiles and clude on anatomical grounds the observation of slow SWS in mammals respond similarly to pharmacological waves in these species (Nieuwenhuys, 1994). In addi- agents (Hartse and Rechtschaffen, 1974, 1982). These tion, it has recently been convincingly argued that the CAT HIPPOCAMPUS 100 mv HIPPOCAMPUS 1s 1s –INTEGRATION TORTOISE LIMBIC AREA 50 mv LIMBIC AREA 1s 1s –INTEGRATION Fig. 7.1. Comparison of mammalian ventral hippocampus spikes in the cat with reptilian spikes in the tortoise. In each record- ing the upper tracing shows the raw, unfiltered record. The lower tracing shows the signal after it has been passed through a bandpass filter set for 30–1000 Hz, a 60-Hz notchfilter, and a Beckman 9852 integrator coupler. Both spikes are shown at slow and fast speeds. (Reprinted with permission from Hartse and Rechtschaffen, 1982.) THE PHYLOGENY OF SLEEP 99 presence of the mammalian neocortex per se is not neurochemical changes (Levenson et al., 1999). Using necessarily the most critical element in the electrophys- time lapse video, preliminary studies in the pond snail, iological expression of slow waves, but rather it is the Lymnaea stagnalis, have identified a resting state advanced development of palliopallial connectivity in which is associated with reduced responsiveness to mammals and birds which accounts for the presence an appetitive stimulus and an increase in quiescence of slow waves in these species (Rattenborg, 2006a). This following rest deprivation (R. Stephenson, personal position has also spurred debate (Rattenborg, 2007; Rial communication). et al., 2007b). In contrast to the findings of SWS asso- Two ocean-dwelling gastropods, the cuttlefish ciated with mammalian and avian quiescence, some (Sepia pharonis) and octopus (Octopus vulgaris), meet investigators have reported the presence of slow waves the criteria for behavioral sleep, and both exhibit during reptilian waking which diminish during behav- rebounds in behavioral sleep following periods of ioral sleep. This observation has been interpreted as sug- enforced wakefulness (Duntley et al., 2002; Brown gesting that reptilian wakefulness, and not reptilian et al., 2006). Electrophysiological recordings from sleep, is the precursor of mammalian SWS (De Vera above the vertical lobe in the brain of the octopus have et al., 1994; Rial et al., 2007a). This position, however, revealed trains of high-amplitude spikes associated has not been widely adopted based upon the preponder- with behavioral quiescence, suggesting a correspon- ance of evidence (Rattenborg et al., 2007). dence to the spikes observed during reptilian behav- As we can see, the task of identifying sleep in non- ioral quiescence (Flanigan, 1973, 1974). A recent