An Objective Behavioral Model of Sleep

Transcription

1 Sleep 11(5): , Raven Press, Ltd., New York 1988 Association of Professional Sleep Societies Theoretical Presentation An Objective Behavioral Model of Sleep Wilse B. Webb Department of Psychology, University of Florida, Gainesville, Florida, U.S.A. Summary: Theories and models are useful in organizing research data. This paper reviews earlier models and a recent model that combines restorative and adaptive models into a two-factor theory. A model emphasizing a three-factor model with modulators is presented as an organizing schema. Key Words: Theory-Sleep-Restorative model-adaptive model. I hope the title of this article has not daunted too many of you. For those of you engaged in the creation of the empirical foundations of the area or others of you who are coping with individuals struggling with disorders of sleep, the world "theory" may raise problems. The term may call forth ideas about air-borne speculations by woolyheaded, ivory-towered types who could not distinguish an electrode from a shoe lace or would be frightened into squeaks by a patient. However, a scientific effort is comprised of three parts: data, application, and theorizing, i.e., the organization and coordination of the data by the use of principles and constructs. A good theory helps us (and others) to better understand and use our data more effectively. It is my purpose today to consider this aspect of sleep research and hopefully to demonstrate the necessary and simplifying role of theorizing. I am made optimistic about this effort by a significant development in sleep theories that has resulted in the reconciliation of two major theoretical positions. I shall briefly review the background of this development and outline its current form. I shall then present my own variation on this model, which I think appropriately extends and emphasizes aspects of that theory. In an earlier review of the extant theoretical positions, I presented five formulations of varying degrees of completeness, independence, and contradictions. Restorative: Sleep is a necessary period of recovery from a state that has been depleted or noxiously developed during waking. These theories emphasized internal state changes. Accepted for publication March Address correspondence and reprint requests to Dr. Wilse B. Webb at Department of Psychology, University of Florida, Gainesville, FL 32611, U.S.A. A version of this paper was presented at the 1987 Elliot Weitzman Memorial Lecture. 488

2 MODEL OF SLEEP 489 Protective: Sleep avoids continued exercise or excessive stimulation. As Claparede put it, sleep does not occur because we are exhausted but to prevent exhaustion. This was at the heart of Pavlov's theory of protective inhibition and sleep. Energy conservation: This position emerged from the empirical relationship between metabolic rates and total sleep time. Smaller animals with high metabolism tended to have higher total sleep time. Thus, sleep was seen to be a form of enforced rest to reduce metabolic requirements. Instinctive: Sleep is viewed as an instinctive expression of innate behavior elicited by "inducing" stimuli. Adaptive theories: Sleep is considered to be an adaptive behavioral responses associated with predator/predatee and foraging requirements of species. These theories focused on sleep amount, period length, and timing of sleep and emphasized environmental determinants. These were not discrete positions and were implicitly and explicitly combined in various ways. For example, Pavlov's protective theory contained a recovery component, and energy conservation theories could be viewed as a special form of a protective theory. Moruzzi's instinctive theory was combined with a restorative model. My own earlier adaptive theorizing was combined with an instinctive position. When examined closely, two major oppositional positions were apparentrestorative and adaptive models. A brief examination of these, however, reveals their limitations. Both positions fit parts of the empirical facts of sleep well. The restorative theories accounted for many of the impelling facts of sleep deprivation and sensibly fit the commonsensical truths of "sleep that knits the raveled sleeve of care." The adaptive theories neatly accounted for the wide ranges of animal sleep in environmental terms. However, both suffered empirical embarrassments. The most reasonable recovery models of sleep would have sleepiness linearly increasing across time and recovery time being some direct function of wake time. However, it was quite clear that sleepiness developed in a wave-like fashion. It was also apparent that recovery time within and across species was not a simple relationship. Within species, the longer waking individual recovered in the shorter time periods, and across species, many animals recovered from 20 h of daily wakefulness in 4 h and others required 18 h to recover from 6 h of wakefulness. Most crucially, this model was hopeless in studies involving sleep displacement. When sleep was shifted from night to daytime, the daytime sleep with equal amounts of prior wakefulness was quite different. The adaptive models, perhaps to distinguish themselves from the recovery models, tended to eschew need/restorative notions and were faced with the intractable facts of increasing sleepiness associated with sleep loss. Furthermore, as it was pointedly noted, rest was certainly more adaptive than sleep, thus making sleep unnecessary. Both suffered crucial theoretical problems with their hypothetical constructs. Simply, neither could empirically specify in a predictive (thus testable) fashion the ostensible "mechanism" underlying their theory. Thus, for the restorative theories, the "substance" or "juice" being depleted could not be identified and its time course specified. For the adaptive theories, the behavioral control mechanism needed to account for the variations in sleep amounts and placements could not be specified in a predictive fashion. Through the 1970s, the theoretical arguments, when of concern, were fitfully restated with little clarification. Fortunately, empirical research proceeds in absence of over-

3 490 W.B. WEBB arching theories. In the 1960s, generally independent of such considerations, a development began within the sleep domain that would markedly affect the general conception of sleep. The techniques, procedures, and findings of chronobiology or biological rhythms began to slowly infuse sleep research. From studies in time-free environments and displaced sleep designs, such as shift work studies, it became increasingly apparent that sleep behavior was significantly determined by an endogenous timing system. Simply, it became clear that sleep, at least partially, was time determined or a circadian biological rhythm. From my perspective within the adaptive theory position, it was increasingly clear that this construct, a biological rhythm, could be appropriately considered the "mechanism" underlying the "adaptive" timings of sleep in coordination with the environment. Light/dark changes were associated with environmental survival advantages and disadvantages, such as predators, foraging, and territorial distributions, and these "placed" sleep and waking activities. Beginning in the 1970s, Alex Borbely and the group in Zurich began explorations of a two-factor theory of sleep. Based on elegant experiments with both animals and humans, they related sleep need, primarily indexed by slow wave sleep (SWS) indices, to time of prior wakefulness and sleep time and conjoined this with the developing research on circadian rhythms that were related to sidereal time. In 1984, Borbely outlined the details of this formulation with his colleague Beersma and one of the outstanding rhythm theorists, Serge Daan (1). The overall aspects of this theory are presented in Fig. 1 from that paper. As can be seen in this figure, there is a sleep need (S) process that arises during wakefulness and diminishes during sleep. This interacts with a circadian system (C) that oscillates on a circadian time scale. These tendencies combine in resultant sleep-wake tendencies in relation to sleep (H) and wake (L) thresholds. In an "entrained" 24-h day, the rise in sleep need (S) coincides with the circadian timing (C) at the sleep threshold (H), and sleep tendencies are maximum. The reversal or decline of S and the rise of the circadian function (C) occurs during sleep, and waking coincides with the waking threshold (L). An important aspect of this theory is seen at the upper right of this figure, "conscious decisions." These are hypothesized as affecting the sleep and waking thresholds (H and L, respectively). Thus, we may elevate the sleep threshold (H), and the sleep need will continue to rise. However, there will be an oscillation ofthe sleep tendencies as a result of the oscillation of the sleep tendencies as a function of the circadian (C) factor. This model clearly fits the rise of sleep tendencies within an entrained circadian day and the decline of sleep tendencies associated with sleeping. By the incorporation of a circadian factor, it can account for the empirical oscillation of sleep tendencies as wakefulness is extended as a result of the interaction of rising sleep demand with the oscillating circadian factor. This incorporation of the circadian factor also provides an effective model for displacement designs such as shift work schedules. If, by "conscious decisions," sleep onset is displaced so that sleep occurs during the low point of the circadian oscillation, say 7:00 a.m. rather than 11:00 p.m., a conflict of C and S tendencies will result in predictable sleep consequences. The model that I am presenting is completely compatible with that proposed by Borbely et al. I have labeled it an "objective behavioral model" of sleep, as this describes its domain and gives due homage to the approach of Clark L. Hull that I was taught in graduate school.

4 MODEL OF SLEEP 491 EXTERNAL CONDITIONS ~) affects synchronizes PHYSiOlOGICAL. OSCILLATKJNS masks e.g., TEMPERATURE, HORMONES, FIG. 1. Daan/Beersma/Borbely model. See text for explanation. CIRCADIAN SLEEP WAKE CYCLE b The domain of concern is an attempt to provide a model for the prediction of sleep as a behavioral event. The bases of these predictions are set in terms of objectively measurable antecedents and concomitants. The format of the model is the approach espoused by Clark L. Hull, which he outlined in his book Principles of Behavior (2), where he proposed an "objective theory of behavior." His aim was to elaborate "the basic molar laws underlying the 'social' sciences." There is little doubt that Hull's aim far exceeded his grasp and that the Hullian theory is a historical relic among the "grand" behavioral theories of the 1930s and 1940s. However, Hull's failure does not necessarily invalidate his approach. It was, after all, modeled on the highly successful Newtonian model of the physical sciences, which was (and remains) a powerful model for comprehending and predicting the molar aspects of the physical world. The essence of the approach is straight-forward and explicit. It is a hypotheticodeductive model based on empirical observations, and "explanation" is defined by the accuracy of predictions made on the basis of "laws" and "principles" underlying the observations. At a theoretical level, observations and their interrelationships are organized as principles or theorems that presumably underlie these relations. These are tested and rejected, modified or elaborated on the basis of their predictive strength. To be emphasized is the procedure by which a construct is introduced. Although the scientist may chose the level of observations (microscopic to macroscopic), the inferred

5 492 W.B. WEBB I '1 processes or constructs must be anchored in observable terms of both the antecedent or consequence. My variation of the Borbely, Beersma, and Daan model is presented in Table 1. As can be seen in this table, the dependent variable is sleep behavior (R sleep), which is, in part, indexed by sleep onset and termination. These variables, in turn, define the presence or absence of sleep and such subsidiary variables as sleep latency, length of sleep, amount, and placement of sleep in the 24-h period. The dependent variables also include sleep structure, which is measured by sleep stages and continuity (awakenings within sleep). In addition, the dependent variables include subjective sleep-related responses subsequent to sleep (sleep evaluations) and within sleep (dream reports, cognitions, and thresholds). This complex of sleep-related measures are hypothesized to be a function of three primary "intervening variables" or dispositional constructs: sleep demand, circadian tendencies, and behavioral facilitators and inhibitors. Each of these variables, in turn, is defined in observable (or potentially observable) terms. Sleep demand is indexed by the time of wakefulness preceding sleep and is a positive exponential function of time. It will be noted that this is simply a time variable and does not include variations of activities in time. A second component of sleep demand is that it is a negative exponential function of time asleep. I consider this last to be a provisional statement in the face of increasing evidence that this may have to be modified to take into account the continuity of sleep. Circadian tendencies are indexed by the timing of sleep within a 24-h matrix. The specific "laws" underlying the tendencies are likely to be complex. For example, the tendencies holding within an entrained 24-h environment we know must be modified under "time-free" or "free-running" environments. Or, as we know, those circadian tendencies present on the first night after a sleep displacement from the entrained sleep time will be different from the predisplaced tendencies and will be modified under continued entrainment in the displaced condition. Behavioral facilitators and inhibitors are likely to be yet more complex. They refer to individual behaviors that facilitate or inhibit the sleep response. In a simple illustration in humans, sleep is facilitated by the prone position and inhibited by an erect position. More complexly, as examples, sleep may be inhibited by behaviors resulting from noises, or incompleted "day residues," or pain and may be facilitated by relaxation or by monotonous nondemanding stimuli. Two facts must be noted. These behaviors may be voluntarily or involuntarily determined, and they are under the control of a complex set of antecedent variables. They mayor may not be "conscious decisions." One may lie down on the basis of habits, urging, fatigue, or boredom. One may not lie down due to a complex variety of ante- 1) I 1 TABLE 1. An objective behavioral model of sleep ~ R sleep = f Sleep demand x circadian tendencies ± behavioral facilitators and inhibitors R sleep = Sleep onset, sleep termination, sleep structure (stages and continuity), and subjective responses Sleep demand = f(positive) wakefulness time and (negative) sleep time Circadian tendencies = f circadian time of sleep Behavioral facilitators and inhibitors = f Voluntary and involuntary, compatible and incompatible with sleep responses These primary variables are modulated by species differences, developmental status, organismic states, and individual differences

6 MODEL OF SLEEP 493 cedents and states: anxiety, work demands, stimulating needs, etc. In short, sleep behavior may be delayed, interrupted or terminated, or facilitated by a vast range of voluntary or involuntary, consciously or unconsciously determined responses. All, however, are potentially measurable in their relationship to the facilitation or inhibition of sleep. The model then specifies that, with the measurement of these three variables and the specification of the laws relating these variables to the sleep behaviors, accurate prediction could be made, for example, in the case of the young human adult. Or, if one controls two of these variables, such as circadian time and behavioral factors, sleep would be a direct function (predictable from), sleep demand. To relieve us from the abstract and to illustrate that many of the laws underlying this model are already present, Figs. 1 and 2 display applications of the model. Figure 1 presents the "prediction" of sleep latency as a function of sleep demand (indexed by the amount of prior wakefulness) with "time to sleep" (circadian time) and behavioral tendencies held constant by laboratory sleep conditions. Figure 2 illustrates the "prediction" of sleep stages as a function of sleep demand (indexed by ongoing sleep time) with similar controls. In a more general situation, we may illustrate the functional aspects of these primary determinants by considering the probability of a nap occurring. If there is a high sleep demand level (up the night before), and it is mid afternoon (there is good evidence of a circadian effect at this time), and the lecture is not eliciting high attending behavior (behavioral facilitation), a nap is predicted. If on the other hand, there is a low sleep demand (awakening at 8:00 a.m. after a good night's sleep), it is 10:00 a.m., and the person is preparing a lecture, a nap is not predicted. The preceding statements explicitly or implicitly are only referent to "human adults." To make the model more comprehensive, additional variables are required. The empirical data of our research makes clear that the three primary variables are modulated by four additional variables: species differences, developmental stages, organismic states, and individual differences. 40 ~, I <h c E > u z UJ f- <l -l a.. ILl ILl 10 -l (J) HOURS PRIOR WAKEFULNESS FIG. 2. Prior wakefulness and sleep onset time (from reference 3).

7 494 W. B. WEBB STAGE REM - :.. ) j:.. STAGE STAGE 2 25 CJ) w 20 I- ::J Z ~ ~.'. :, :... " HOURS OF SLEEP FIG. 3. Sleep stages and time asleep (from reference 4). Between species there is a wide range of sleep demand levels, circadian tendencies, and behavioral repertoires. Very simply, elephants sleep like elephants, rats like rats, and humans like humans. More specifically, sleep demands vary widely. For example, grazing animals, in general, sleep between 2 and 4 h in brief bursts across the 24 h, whereas smaller animals, such as rodents, sleep 12 h or more and primates tend to sleep in intermediate amounts. Similarly, circadian tendencies show wide ranging patterns that include nocturnal, diurnal, and acircadian distributions. There are also different behavioral repetoires. For each species then, for each of the primary determinants, different values must be determined and assigned for predictive purposes. The sleep of the rat, for example, does not rise exponentially across 16 h and decline across 8 h. Rather, it must be heavily weighted in the "light-time" hours and timed in intermittent bursts. Sleep demand is approximated at 12 h, and the behavioral facilitator and inhibitors are heavily determined by natural environmental cues. It is further apparent that the primary variables are responsive to developmental stages. Again, very simply, babies sleep as babies, adults as adults, and older persons as older persons. In humans, sleep demand varies from an average of some 16 hi24 in infants to half that amount in adults. Circadian tendencies move from an acircadian, polyphasic pattern at birth, through nap patterns, and back to nap patterns in the elderly. And certainly the prone behavior of the infant is vastly different from the active adult. These differences are modulators of the three primary variables. All sleep variables are, of course, mediated by organismic states. In this formulation, however, I am referring to those objectively identified induced or extant states that have been shown to modulate one or more of the primary variables. These would Sleep, Vol. JI, No.5, 1988

8 MODEL OF SLEEP 495 include pharmaceutically or biochemically induced states associated with, for example, sleeping pills or central nervous system (ens) activators, such as caffeine. These would also include pathologic conditions as narcolepsy or sleep apnea. Finally, for the crucial matter of individual predictions, individual differences must be included. Within any species, developmental stage, or organismic state, the primary variables show a range of individual differences. Again, as an illustration, relative sleep demand averages about 7.5 h across human adults. However, the standard deviation is about 1 h. In short, there are relatively stable individual levels of sleep demand ranging from about 4.5 h to 10.5 h. Though less clearly defined, it is clear that systematic individual variations are present in circadian tendencies and behavioral tendencies. In the prediction of individual behaviors, the primary variables must be "modulated" to reflect the individual tendencies of each individual. From these considerations, it follows that the prediction of sleep behaviors is a formidable but sensible process. To make such a prediction, one must specify the primary variables: sleep demand, circadian tendencies, and behavioral facilitators and inhibitors. We must, in addition, specify the species, developmental status, organismic state, and individual tendencies. With what we know about these variables, particularly in that well-studied species human kind, with such specifications we can make remarkably good predictions about a range of sleep behaviors. For example, regarding sleep onset or sleep structure, specifying time awake (sleep demand), sidereal time (circadian tendencies), and the behavioral conditions (facilitors and inhibitors) and referencing a human who is 60 years old, normal, and drug-free and with a knowledge of his repetition tendencies, we can speak with some accuracy and confidence about how quickly that person will go to sleep, what the structure of that sleep will be, and when the person will awaken. Without such specifications and our body of research, we must resort to necromancy or fraud. What may be said about this particular model? First, as noted, it is compatible with the Borbely, Beersma, and Daan model. As a consequence, it carries the major theoretical advantage of incorporating sleep demand and circadian tendencies. As such, like their model, it reconciles the two major competing theoretical positions and yields both their strengths in predicting sleep behaviors. It is far less elegant, in its present form, in the interactive relations of these components relative to such constructs as thresholds. As a consequence, it is less capable of being tested with precision. This, of course, gives to my model an unfair advantage. There is an old adage in theory building that the less testable a model, the longer is its probable lifespan. I believe that the broadening and emphasizing of their construct of "conscious decisions" to include the broader range of behavioral facilitators and inhibitors is not only desirable, but also crucial. These processes are preeminent and necessary considerations in predicting the probability (and improbability) of sleep and can be better operationally defined than "lurking" cognitive states. In short, I am espousing and advocating a three-factor, rather than a two-factor, model. The incorporation of the four modulators-species, age, organismic states, and individual differences-gives due emphasis to variables that have been experimentally demonstrated to be crucial determinants of the sleep responses. However, the primary purpose of this exercise has been to try to fulfill one of the heuristic roles of modeling or theorizing-that of organizing our multitudinous facts into a relatively simple, coherent, understandable whole. Sleep, Vol. 11. No.5, 1988

9 496 W.B. WEBB Nearly 20 years ago, in a small book titled Sleep: An Experimental Approach (5), I wrote: it has been my experience that data gathering in absence of theory or concepts may result in a mound of facts which often miss ultimate causes or effects or indeed may bury them... It seems, however, that the time is approaching when we shall be increasingly certain of our facts, and our concepts and theories will become more sophisticated and clear. At this point, we shall begin to see more clearly the multilevel causes of sleep ranging from genetic influences and early training to immediate environmental influences as well as biochemical factors. In addition, we shall be able to specify the resultant effects of sleep at levels ranging from neurobiological and cellular to psychological and behavioral. (p. 56) There is little doubt that our facts have continued to burgeon. The last publication of Sleep Research (6) presents an annual yield of 651 abstracts presented at the annual meeting and 1,882 bibliographic citations. The citations are over an incredible range of topics from single nerve cell to jet lag, from cockroaches to apneas, from drugs to dreams. However, I fear that this outpouring presents problems as well as opportunities. To quote another favorite author (7): (In modern science) inductive data fall upon us from all sides like the lava from Vesuvius; we suffocate with uncoordinated facts; our minds are overwhelmed with science breeding and multiplying in specialist chaos for want of synthetic thought. (p. 91) Hopefully, such a schema as I have presented, and more sophisticated ones that may follow, will didactically aid us in seeing these data in a way that will let us view our, individual efforts in a more comprehensive framework and help us to communicate this I grand enterprise to our students, consumers, and the general public. A final comment is in order. Relative to sleep research, the model presented can only be viewed as chapter 1. It is a treatment of sleep as a dependent variable, i.e., the prediction of sleep as a function of antecedent and concomitant variables. Chapter 2 must encompass sleep as an independent variable. This must systematically organize the relationships between variations in sleep relative to the consequences. Hopefully,.~ here we can organize our multifarious finding relative to sleep loss (partial, total, and selective), sleep continuity, sleep displacement, dreams, and sleep-induced neurophysiologic variations in terms of their relationship to our waking life. REFERENCES 1. Daan S, Beersma DGM, Borbely AA. Timing of human sleep: recovery process gated by a circadian pacemaker. Am J PhysioI1984;246:RI Hull CL. Principles of behavior. New York: Appleton-Century, Agnew HW, Webb WB. Sleep latencies in human subjects: age, prior wakefulness and reliability. Psychnom Sci 1971;24: Webb WB, Agnew HW. Analyses of sleep stages in sleep wakefulness regimens of varied length. Psychophysiology 1974;14: Webb WB. Sleep: an experimental variable. New York: Macmillan, Chase M, McGinty D (eds) Sleep Research, 1987, Vol Durant W. The story of philosophy. New York: Washington Square Press, 1961.