Neural basis of timing and anticipatory behaviors

Abstract

The ability to anticipate physiological needs and to predict the availability of desirable resources optimizes the likelihood of survival for an organism. The neural basis of the complex behaviors associated with anticipatory responses is now being delineated. Anticipation likely involves learning and memory, reward and punishment, memory and cognition, arousal and feedback associated with changes in internal and external state, homeostatic processes and timing mechanisms. While anticipation can occur on a variety of timescales (seconds to minutes to hours to days to a year), there have been great strides made towards understanding the neural basis timing of events in the circadian realm. Anticipation of daily events, such as scheduled access to food, may serve as a useful model for a more broadly based understanding the neurobiology of anticipation. In this review we examine the historical, conceptual and experimental approaches to understanding the neural basis of anticipation with a focus on anticipation of scheduled daily meals. We also introduce the key topics represented in the papers in this issue. These papers focused on food anticipation, to explore the state of the art in the studies of the neural basis of timing and anticipatory behaviors.

Figure 1

A model of how various systems regulate anticipation. Anticipation is a function of cognitive processes such as learning and memory, as well as unconscious processes such as underlying oscillators, interval timers and arousal. Homeostatic drives may be considered a special case of interval timers that help maintain physiological set-points by steadily increasing drive states as time passes and, upon reaching a threshold, trigger a response. The event anticipated can feedback to each of these processes: It can provide an event to be remembered, set the phase of an oscillator, reset an interval timer, alter a homeostatic drive and influence arousal. Furthermore, all the processes that feed into anticipation may interact.

Figure 2

Various tissues in the body can exhibit circadian oscillations. The suprachiasmatic nucleus (SCN) is the master light-entrainable pacemaker and under normal physiological conditions sets the phase of other oscillators in the brain and body, such as the liver and bed nucleus of the stria terminalis (BNST), each of which can have its own phase, distinct from that of the SCN. When subjected to a restricted feeding protocol, many peripheral oscillators have their phase reset, such that they acquire a particular phase angle relative to feeding time. Some tissues, such as the dorsomedial hypothalamus (DMH) only exhibit strong oscillations when the individual is on a scheduled feeding regimen.

Figure 3

The light entrainable pacemaker in the suprachiasmatic nucleus receives light information from the retina from the retinohypothalamic tract (yellow). The SCN sets the phase of various peripheral oscillators (blue). When individuals are placed on restricted feeding schedules, the phases of peripheral “food-entrainable oscillators” are adjusted to track feeding time (green). There may be communication between food entrainable oscillators in the brain and periphery (red). See the literature cited in the text for details.

Figure 4

Some aspect of Borbely’s two-process model of sleep regulation may also apply to circadian/homeostatic regulation of FAA. A circadian component (C) provides thresholds for wake (lower oscillation) and sleep (upper oscillation) onset. During wake, a homeostatic sleep drive (S) increases. When the sleep drive intersect with the circadian rhythm for sleep onset, sleep is initiated, and the homeostatic drive decreases during the sleep, until it intersects with the circadian rhythm for wake onset, at which point the individual awakens, and the cycle reinitiates. Modified from (Daan et al., 1984).