PHYSIOLOGICAL REVIEWThermoregulation as a sleep signalling system
Section snippets
Human thermoregulation
Thermoregulation refers to the processes required to maintain the body temperature within a narrow set range essential for cell functioning. One of the first models of temperature regulation was formulated by Aschoff in 19561 and incorporated the idea of a core and a shell. In such a model, the temperature of the core (TC) is maintained within a specific range (around 37 °C). In contrast, the shell is dependent largely on environmental temperature with the extremities of the body, such as the
Autonomic aspects of temperature regulation
Although temperature can be influenced by conscious actions, nearly all of the highly specific and subtle day-to-day processes involved in thermoregulation are unconscious and controlled by the autonomic nervous system.3 Information about environmental temperature or the temperature of objects is registered by receptors in the skin. These thermoreceptors fall into two general categories: cold receptors or those that detect changes in temperature in the order of 20–30 °C, and warm receptors
Servocontrol or ‘set point’ model of temperature regulation
Although the exact mechanism by which the PoAH maintains precise control over body temperature is unclear, one of the more accepted models incorporates the idea of a set point and the concepts and terminology of servocontrol systems typically used in the field of engineering. In such a model, core body temperature is maintained within a specific range by comparing the moment-to-moment temperature with a desired value or set point by the PoAH. The PoAH then generates an error signal that is
The circadian regulation of temperature
The principles of thermal homeostasis described above enable the body to respond appropriately to acute changes in the environment. In addition, thermal homeostasis has a temporal aspect that facilitates the prediction of environmental challenges, thereby allowing corrective responses to such challenges to occur in advance. This concept of predictive homeostasis is clearly represented in the thermal physiology of the circadian system.
In healthy individuals, (TC) demonstrates predictable
Regulation of the sleep/wake cycle
While the rhythm of TC is one of the most well recognised circadian rhythms, many physiological processes and behavioural functions, including sleep, are circadian in nature. In order to determine which aspects of sleep are influenced by the circadian system, experimental protocols have been developed in which an individual's sleep/wake cycle becomes disassociated from circadian control.12., 13. Of these experimental protocols, one of the most common designs is called a forced desynchrony
Relationship between sleep and temperature
Historically, changes in TC accompanying changes in sleep propensity have typically been attributed to the influence of the circadian system on sleep. This belief was a consequence of the association between the timing of sleep onset and changes in TC consistently observed under temporal isolation and in forced desynchrony protocols. However, as will be discussed in following sections, a clear relationship between these variables also exists under a wide range of experimental conditions where
Changes in temperature following sleep onset
Despite the current interest in the relationship between sleep propensity and temperature, the association between sleep, in general, and temperature has been recognised for many years. For example, in the early 20th century there was some debate as to whether the nocturnal reduction in TC was a result of sleep itself or simply due to a change in posture. From initial studies, it was concluded that, provided subjects remained still and quiet in bed, neither sleep nor waking affected temperature.
Thermoregulatory changes following sleep onset
As interest in the relationship between thermoregulation and sleep developed, experiments were conducted to determine the effects of ambient temperature on sleep quality (which includes factors such as SOL, total sleep time, nocturnal arousals, amount of SWS and the amount of rapid eye movement sleep).28., 29., 30., 31., 32., 33., 34. Not only did these experiments provide insight into the role of temperature in the progression between sleep states (e.g. NREM-REM; see Ref. [29] for review), but
The effects of pharmacological manipulations of sleep on temperature: A causal relationship between temperature and sleep propensity?
Not only are there clear examples of temperature affecting sleep onset itself, but also changes in temperature are highly correlated with the likelihood of falling asleep. In recent times, thermoregulatory effects have been documented following the administration of sedative-hypnotic and also alerting agents. For example, somnogenic agents such as melatonin41., 42., 43., 44., 45. and benzodiazepines46., 47., 48. increase sleep propensity while decreasing TC. In contrast, agents such as
Integrating the effects of sleep-on-temperature with the effects of temperature-on-sleep
It is clear that temperature and sleep are closely interlinked under a wide range of situations. This has resulted in considerable debate as to the possible mechanisms driving these changes in temperature and sleep. One of the central themes in this debate has been the question of whether the relationship between sleep propensity and TC reflects circadian control or reflects a causal relationship between the two variables. There is no doubt that, under normal conditions, the primary factor
The role of the PoAH and thermosensitive neurones in sleep regulation
Neuroanatomical research revealed that sleep could be initiated following physical warming of the PoAH52., 53. and also following chemical stimulation of the same area.54 Such a finding implicated activation of the PoAH in the normal initiation of sleep. Consistent with such a hypothesis, groups of warm-sensitive neurons in the PoAH were found to increase their firing rate at sleep onset and decrease their firing just before arousal in animals,55 an observation confirmed by immunocytochemistry.
A model of sleep regulation
Integrating the available neuroanatomical and physiological research, a model is proposed below to explain how an increase in peripheral heat loss, whether by pharmacological manipulation, exercise, or hot baths, is able to increase sleepiness. In addition, the role of temperature changes following sleep onset in the regulation of sleep will be explained. This model is schematically illustrated in Fig. 4. While previous authors such as van Someren60 have proposed a mechanism through which the
Thermoregulatory changes in sleep disorders
The above sections have summarised the effects that manipulations of TC have on sleep and have highlighted a potential role of a rapid decline in TC and an increase in heat loss in sleep initiation. Interestingly, investigation of the thermoregulatory changes associated with several sleep disorders also provides indirect support for a role of thermoregulatory changes in sleep propensity. For example, sleep onset insomniacs have been found to have a delay in their TC rhythm of approximately 2.5
Conclusion
It is apparent that thermoregulatory variables such as TC and peripheral heat loss are associated with sleep propensity under a wide range of experimental situations. It also appears that the thermoregulatory control centre, the PoAH, is not only directly involved in the regulation of sleep and wakefulness, but also innervates other somnogenic brain regions. Taken together, it is possible that, in addition to other systems such as the circadian system, the thermoregulatory system may act as a
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