Heat Synch: Inter- and Independence of Body-Temperature Fluctuations and Brain-State Alternations in Urethane-Anesthetized Rats

Abstract

During sleep, warm-blooded animals exhibit cyclic alternations between rapid-eye-movement (REM) and nonrapid-eye-movement (non-REM) states, characterized by distinct patterns of brain activity apparent in electroencephalographic (EEG) recordings coupled with corresponding changes in physiological measures, including body temperature. Recently we have shown that urethane-anesthetized rats display cyclic alternations between an activated state and a deactivated state that are highly similar in both EEG and physiological characteristics to REM and non-REM sleep states, respectively. Here, using intracranial local field potential recordings from urethane-anesthetized rats, we show that brain-state alternations were correlated to core temperature fluctuations induced using a feedback-controlled heating system. Activated (REM-like) states predominated during the rising phase of the temperature cycle, whereas deactivated (non-REM-like) states predominated during the falling phase. Brain-state alternations persisted following the elimination of core temperature fluctuations by the use of a constant heating protocol, but the timing and rhythmicity of state alternations were altered. In contrast, thermal fluctuations applied to the ventral surface (and especially the scrotum) of rats in the absence or independently of core temperature fluctuations appeared to induce brain-state alternations. Heating brought about activated patterns, whereas cooling produced deactivated patterns. This shows that although alternations of sleeplike brain states under urethane anesthesia can be independent of imposed temperature variations, they can also be entrained through the activation of peripheral thermoreceptors. Overall, these results imply that brain state and bodily metabolism are highly related during unconsciousness and that the brain mechanisms underlying sleep cycling and thermoregulation likely represent independent, yet coupled oscillators.