Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle

Abstract

Brown adipose tissue (BAT), body and brain temperatures, as well as behavioral activity, arterial pressure and heart rate, increase episodically during the waking (dark) phase of the circadian cycle in rats. Phase-linking of combinations of these ultradian (<24 hour) events has previously been noted, but no synthesis of their overall interrelationships has emerged. We hypothesized that they are coordinated by brain central command, and that BAT thermogenesis, itself controlled by the brain, contributes to increases in brain and body temperature. We used chronically implanted instruments to measure combinations of BAT, brain and body temperatures, behavioral activity, tail artery blood flow, and arterial pressure and heart rate, in conscious freely moving Sprague-Dawley rats during the 12 hour dark active period. Ambient temperature was kept constant for any particular 24 hour day, varying between 22°C and 27°C on different days. Increases in BAT temperature (≥0.5°C) occurred in an irregular episodic manner every 94±43 min (mean±SD). Varying the temperature over a wider range (18-30°C) on different days did not change the periodicity, and neither body nor brain temperature fell before BAT temperature episodic increases. These increases are thus unlikely to reflect thermoregulatory homeostasis. Episodic BAT thermogenesis still occurred in food-deprived rats. Behavioral activity, arterial pressure (18±5 mmHg every 98±49 min) and heart rate (86±31 beats/min) increased approximately 3 min before each increase in BAT temperature. Increases in BAT temperature (1.1±0.4°C) were larger than corresponding increases in brain (0.8±0.4°C) and body (0.6±0.3°C) temperature and the BAT episodes commenced 2-3 min before body and brain episodes, suggesting that BAT thermogenesis warms body and brain. Hippocampal 5-8 Hz theta rhythm, indicating active engagement with the environment, increased before the behavioral and autonomic events, suggesting coordination by brain central command as part of the 1-2 hour ultradian basic rest-activity cycle (BRAC) proposed by Kleitman.

Brown adipose tissue thermogenesis contributes to emotional hyperthermia in a resident rat suddenly confronted with an intruder rat

“…Instrumented rats were transferred to the residence cage and housed individually for at least 1 day before the intruder experiments were conducted. During this 24-h period the resident rat displayed episodic ultradian increases in BAT, body, and brain temperatures preceding food intake, with episodes occurring at ϳ90-min intervals as we previously reported (3,46). We introduced the intruder rat during the dark phase ϳ20 min after the end of a meal when the rat was inactive and BAT, body, and brain temperatures were at low levels.…”

“…In the present study we observed the resident rat for at least 24 h, recording the coordinated behavioral and physiological events that occur when the rat engages with the external environment as part of the basic rest-activity cycle (2,3,46,47). This enabled us to introduce the intruder rat when temperatures were at a basal level.…”

“…Measurement of physiological and environmental variables. With the use of general anesthesia as described above, precalibrated thermistor probes (3,46) were positioned in interscapular BAT near the vein of Sulzer (BAT temperature), in the anterior mediastinum ventral to the trachea (body temperature), and intracranially near the junction of sagittal and transverse sinuses, between the dura mater and the skull bone (brain temperature). We chose this extradural site to minimize traumatic damage associated with intracerebral probes.…”

Novel energy-saving strategies to multiple stressors in birds: the ultradian regulation of body temperature

“…A well-recognized metabolic adaptation to fasting is the reduction in heat production [6,7], accompanied by reductions in T b , usually through progressive declines during the inactive period [8][9][10][11][12][13][14], which have been argued to result from a regulated thermoregulatory response [8,9,15,16]. Fluctuations in T b can result from changes in set point [17,18], changes in activity [19,20] or changes in thermal conductance [21]. In birds, regional heterothermy during fasting may provide an explanation for why core T b does not vary much with fasting in some species, despite a large metabolic suppression [21].…”

“…Although these fluctuations may simply appear to be noise, they have important physiological signatures (e.g. insulin and growth hormone show pulsatile secretion in phase with T b fluctuations [24,25], fluctuations in core T b of quail are associated with changes in fuel use [26], alterations in hippocampal activation precedes thermogenic fluctuations [19,20]). As altered vigilance behaviours (i.e.…”