The enigma of behavioral inputs to the circadian clock: a test of function using restraint

Wheel running stimulated during the daily rest period can acutely shift circadian rhythms in Syrian hamsters. Spontaneous running, defining the active phase of the circadian rest-activity cycle, can shorten the circadian periodicity in constant light or dark in several nocturnal rodent species. The adaptive significance of these behavioral effects on pacemaker phase and period is unclear. Here we consider a hypothesis that behavioral inputs to the circadian pacemaker serve primarily to enhance the precision of light-dark entrainment and maintain daily activity onset close to lights-off (i.e., dusk) by stabilizing entrainment on a steeper portion of the delay zone of the phase-response curve to light. This hypothesis rests on the evidence that spontaneous activity early in the active period feeds back on the pacemaker to advance its motion. If so, then preventing activity at this time should induce a phase delay shift. Such delay shifts have been reported in Syrian hamsters physically restrained early in the active period. We show here that restraint can induce phase delays but that, using the Aschoff Type 2 procedure for measuring shifts, these delays are very small, are inversely related to behavioral sleep during restraint, and are positively correlated with 'rebound' increases in running following restraint, at a circadian time when stimulated running is known to induce phase delay shifts. Repeated bouts of restraint, to promote habituation, were associated with strong attenuation of 'rebound' running and no significant delay shifts. These results suggest that, in Syrian hamsters, spontaneous activity early at night has little effect on pacemaker motion, and argue against the stated hypothesis.