Brain control of body temperature: Central command vs feedback

In his landmark Physiological Reviews article of 1929 Walter Cannon defined homeostasis as the coordinated physiological mechanisms that maintain the physical and chemical properties of the internal environment, i.e. the extracellular fluid that surrounds all cells in the body. This in turn was based on the principle, first enunciated by Claude Bernard, that the constancy of the internal environment is essential for the survival of organisms. Modern physiology textbooks typically begin with a discussion of the principles of homeostasis, and often explain these as analogous to physical feedback control systems. Thus, the body system maintaining body temperature is often likened to a thermostat that maintains a constant room temperature. According to this scheme, the body detects deviations in temperature from some desired constant setpoint, and then generates physiological changes that return the temperature to the setpoint. The difficulty with this scheme, as pointed out by Blessing and Ootsuka in their article “Timing of activities of daily life is jaggy: How episodic ultradian changes in body and brain temperature are integrated into this process” published in this issue, is that continuous measurements of temperature in the body core or brain show that changes in body temperature frequently occur that cannot be explained by feedback regulation around a constant setpoint. For example, as illustrated in Figure 2 in their article, there are distinct episodes, occurring on average every 1–2 hours, in which the body and brain temperature of a rat is increased by 1 C or more for periods ranging from a few minutes to about 30 minutes, even under conditions where the rat is in a quiet environment with controlled ambient temperature, and with ad libitum access to food and water. The increases in temperature were accompanied by increases in the temperature of brown adipose tissues (BAT) of even greater magnitude, indicating that they occur as a direct consequence of sympathetically mediated BAT thermogenesis. The episodes of increased temperature are part of a patterned coordinated physiological response, since they are accompanied by increases in arterial pressure, heart rate and somatomotor activity, and are interspersed with rest periods. The somatomotor and autonomic changes are preceded by an increase in EEG theta power, suggesting increased engagement with the environment, and typically are followed by increases in eating. Such episodic events that occur more frequently than once every 24 hours are referred to as “ultradian” events, to distinguish them from circadian events that occur once every 24 hours. The coordinated ultradian physiological responses must be driven from the brain, i.e., by central command. Similarly, the immediate coordinated somatomotor and autonomic changes that occur at the onset of exercise, or which are triggered when an animal detects a predator or prey, are also driven by central command. At the same time, reflex compensatory mechanisms that depend upon feedback from peripheral receptors are also an essential part of physiological regulatory systems that ensure the survival of animals in the face of environmental threats or internal challenges. Furthermore, reflex mechanisms and central command are not necessarily independent. For example, during exercise central command signals from the forebrain reset the baroreceptor reflex, such that arterial pressure continues to be reflexly regulated, but around a higher level which is physiologically more advantageous during exercise. As Day has pointed out in an insightful review, Cannon in explaining the concept of homeostasis clearly distinguished between the physiological factors that are critical for cell survival (e.g. nutrient availability, oxygen content, pH, ion concentration and temperature) and those variables that help to maintain these critical factors,