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The Circadian Rhythm of Thermoregulation Modulates both the Sleep/Wake Cycle and 24 h Pattern of Arterial Blood Pressure

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Abstract

Borbély proposed an interacting two‐component model of sleep regulation comprising a homeostatic Process S and a circadian Process C. The model has provided understanding of the association between core body temperature (CBT) as a key element of Process C that is deterministic of sleep onset and offset. However, it additionally provides a new perspective of the importance of the thermoregulatory mechanisms of Process C in modulating the circadian rhythm of arterial blood pressure (ABP). Herein, we examine the circadian physiology of thermoregulation, including at the end of the activity span the profound redistribution of cardiac output from the systemic circulation to the arteriovenous anastomoses of the glabrous skin that markedly enhances convective transfer of heat from the body to the environment to cause (i) decrease of the CBT as a pathway to sleep onset and (ii) attenuation of the asleep ABP mean and augmentation of the ABP decline (dipping) from the wake‐time mean, in combination the strongest predictors of the risk for blood vessel and organ pathology and morbid and mortal cardiovascular disease events. We additionally review the means by which blood perfusion to the glabrous skin can be manipulated on demand by selective thermal stimulation, that is, mild warming, on the skin of the cervical spinal cord to intensify Process C as a way to facilitate sleep induction and promote healthy asleep ABP. © 2021 American Physiological Society. Compr Physiol 11:1‐14, 2021.

Figure 1. Figure 1. 24 h temporal patterns of homeostatic Process S, indicative of sleep pressure level (panel A1), and circadian Process C (panel A2), indicative of the biological readiness for sleep onset and offset (awakening), of the Borbély two‐process model of sleep regulation (modified from Borbély19). Sleep onset and offset are regulated in time during the 24 h through the interaction between the respective threshold levels of Process S and Process C. Panels B to E adopted from van der Heide et al. 126, respectively, illustrate the circadian rhythm of the distal temperature (derived from temperature measurements made at the thenar area of the palmar side of both hands and the medial metatarsal area of the plantar sides of both feet), proximal temperature (derived from temperature measurements of the infra‐clavicular, thigh, and abdominal areas), and the consequently calculated distal‐proximal temperature gradient (DPG) of 8 diurnally active healthy males 37.9 ± 4.1 years of age. Panels F to I adopted from Hermida et al. 56,61, respectively, illustrate the circadian rhythm of heart rate (HR), systolic blood pressure (SBP), diastolic blood pressure (DBP), and double product (SBP × HR, surrogate measure of left ventricular work and myocardial oxygen demand) of 184 diurnally active healthy males 22.4 ± 2.1 years of age. Shaded and nonshaded background of each panel, respectively, indicates the known or assumed sleep and wake spans. The core body temperature (CBT) is a biomarker of Process C. It declines to its threshold in association with the elevation of DPG late in the activity span to enable sleep onset. The decrease of the CBT at this time and throughout sleep coincides with the decrease of SBP, DBP, HR, and HR × SBP. Just prior to sleep offset CBT, SBP, DBP, and HR × SBP rise simultaneously.
Figure 2. Figure 2. Infra‐red images of a subject with probable vasospastic syndrome before and after three different levels of upper cervical spine region thermal stimulation. Left side images (panels, A, C, and E) taken prior to laying supine for 30 min, and the right side top (panel B), middle (panel D), and bottom (panel F) row images taken following, respectively, no, mild (38 °C), and strong (41 °C) STS. In each baseline session, before application of the 30‐minute STS (panels, A, C, and E), the subject displays an abnormally low level of blood flow through the AVA resulting in cold palms of the hands and soles of the feet, which is depicted by the dark black color of the fingers and palms of the hands and soles of the feet. With the application of the mild and strong warming STS to the cervical spine region, the finger and hands (arrow tip of panels B, D, and F) are progressive lighter and brighter in color, which is indicative of the higher blood flow to the AVA and warmer temperature of the glabrous skin of these extremities.


Figure 1. 24 h temporal patterns of homeostatic Process S, indicative of sleep pressure level (panel A1), and circadian Process C (panel A2), indicative of the biological readiness for sleep onset and offset (awakening), of the Borbély two‐process model of sleep regulation (modified from Borbély19). Sleep onset and offset are regulated in time during the 24 h through the interaction between the respective threshold levels of Process S and Process C. Panels B to E adopted from van der Heide et al. 126, respectively, illustrate the circadian rhythm of the distal temperature (derived from temperature measurements made at the thenar area of the palmar side of both hands and the medial metatarsal area of the plantar sides of both feet), proximal temperature (derived from temperature measurements of the infra‐clavicular, thigh, and abdominal areas), and the consequently calculated distal‐proximal temperature gradient (DPG) of 8 diurnally active healthy males 37.9 ± 4.1 years of age. Panels F to I adopted from Hermida et al. 56,61, respectively, illustrate the circadian rhythm of heart rate (HR), systolic blood pressure (SBP), diastolic blood pressure (DBP), and double product (SBP × HR, surrogate measure of left ventricular work and myocardial oxygen demand) of 184 diurnally active healthy males 22.4 ± 2.1 years of age. Shaded and nonshaded background of each panel, respectively, indicates the known or assumed sleep and wake spans. The core body temperature (CBT) is a biomarker of Process C. It declines to its threshold in association with the elevation of DPG late in the activity span to enable sleep onset. The decrease of the CBT at this time and throughout sleep coincides with the decrease of SBP, DBP, HR, and HR × SBP. Just prior to sleep offset CBT, SBP, DBP, and HR × SBP rise simultaneously.


Figure 2. Infra‐red images of a subject with probable vasospastic syndrome before and after three different levels of upper cervical spine region thermal stimulation. Left side images (panels, A, C, and E) taken prior to laying supine for 30 min, and the right side top (panel B), middle (panel D), and bottom (panel F) row images taken following, respectively, no, mild (38 °C), and strong (41 °C) STS. In each baseline session, before application of the 30‐minute STS (panels, A, C, and E), the subject displays an abnormally low level of blood flow through the AVA resulting in cold palms of the hands and soles of the feet, which is depicted by the dark black color of the fingers and palms of the hands and soles of the feet. With the application of the mild and strong warming STS to the cervical spine region, the finger and hands (arrow tip of panels B, D, and F) are progressive lighter and brighter in color, which is indicative of the higher blood flow to the AVA and warmer temperature of the glabrous skin of these extremities.
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Shahab Haghayegh, Michael H. Smolensky, Sepideh Khoshnevis, Ramon C. Hermida, Richard J. Castriotta, Kenneth R. Diller. The Circadian Rhythm of Thermoregulation Modulates both the Sleep/Wake Cycle and 24 h Pattern of Arterial Blood Pressure. Compr Physiol 2021, 11: 2645-2658. doi: 10.1002/cphy.c210008