Abstract
Feeding schedules entrain circadian clocks in multiple brain regions and most peripheral organs and tissues, thereby synchronizing daily rhythms of foraging behavior and physiology with times of day when food is most likely to be found. Entrainment of peripheral clocks to mealtime is accomplished by multiple feeding-related signals, including absorbed nutrients and metabolic hormones, acting in parallel or in series in a tissue-specific fashion. Less is known about the signals that synchronize circadian clocks in the brain with feeding time, some of which are presumed to generate the circadian rhythms of food-anticipatory activity that emerge when food is restricted to a fixed daily mealtime. In this commentary, I consider the possibility that food-anticipatory activity rhythms are driven or entrained by circulating ghrelin, ketone bodies or insulin. While evidence supports the potential of these signals to participate in the induction or amount of food-anticipatory behavior, it falls short of establishing either a necessary or sufficient role or accounting for circadian properties of anticipatory rhythms. The availability of multiple, circulating signals by which circadian oscillators in many brain regions might entrain to mealtime has supported a view that food-anticipatory rhythms of behavior are mediated by a broadly distributed system of clocks. The evidence, however, does not rule out the possibility that multiple peripheral and central food-entrained oscillators and feeding-related signals converge on circadian oscillators in a defined location which ultimately set the phase and gate the expression of anticipatory activity rhythms. A candidate location is the dorsal striatum, a core component of the neural system which mediates reward, motivation and action and which contains circadian oscillators entrainable by food and dopaminergic drugs. Systemic metabolic signals, such as ghrelin, ketones and insulin, may participate in circadian food anticipation to the extent that they modulate dopamine afferents to circadian clocks in this area.
Highlights
Feeding schedules entrain circadian clocks in multiple brain regions and most peripheral organs and tissues, thereby synchronizing daily rhythms of foraging behavior and physiology with times of day when food is most likely to be found
Concluding thoughts This article has served as a vehicle to highlight some unresolved issues in mammalian circadian biology, including the formal structure, molecular and cellular substrates and input pathways of the circadian timing system that synchronizes appetitive behavior with daily rhythms in the availability of food or other strong rewards
The utility of a circadian system for adjusting rest–activity cycles to times of day most favorable for resource acquisition is self-evident, but it is not unreasonable to speculate that clock entrainment could support addictive behaviors
Summary
F1000 Faculty Reviews are written by members of the prestigious F1000 Faculty. They are commissioned and are peer reviewed before publication to ensure that the final, published version is comprehensive and accessible. The subsequent discovery that bona fide circadian FEOs (cells that express clock gene rhythms that are entrained by daily feeding schedules) are found throughout the body[10,17], combined with a lack of success in defining critical neural loci, has renewed interest in peripheral organs and their outputs as sources of timing information for food-anticipatory behavior. Rats can anticipate two daily meals; if one is in the light period and the other at night, peripheral clocks assume an intermediate phase or maintain a nocturnal alignment, depending on the relative meal sizes, intermeal interval, and timing within the day[67,68,69] These dissociations make clear that ghrelin secreted by gastric FEOs does not directly initiate FAA, but the results do not rule out a role for ghrelin as a participant in phase control of FEOs for behavior which are located elsewhere in the body or brain. These converging narratives invite speculation that a common pool of DA-regulated oscillators may underlie behavioral rhythmicity in the ultradian and circadian range and behavioral disorders associated with hyperdopaminergic states
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