Resetting of the hamster circadian system by dark pulses

Abstract

-Circadian rhythms of animals are reset by exposure to light as well as dark; however, although the parameters of photic entrainment are well characterized, the phaseshifting actions of dark pulses are poorly understood. Here, we determined the tonic and phasic effects of short (0.25 h), moderate (3 h), and long (6 -9 h) duration dark pulses on the wheel-running rhythms of hamsters in constant light. Moderate-and long-duration dark pulses phase dependently reset behavioral rhythms, and the magnitude of these phase shifts increased as a function of the duration of the dark pulse. In contrast, the 0.25-h dark pulses failed to evoke consistent effects at any circadian phase tested. Interestingly, moderate-and long-dark pulses elevated locomotor activity (wheel-running) on the day of treatment. This induced wheel-running was highly correlated with phase shift magnitude when the pulse was given during the subjective day. This, together with the finding that animals pulsed during the subjective day are behaviorally active throughout the pulse, suggests that both locomotor activity and behavioral activation play an important role in the phase-resetting actions of dark pulses. We also found that the robustness of the wheel-running rhythm was weakened, and the amount of wheel-running decreased on the days after exposure to dark pulses; these effects were dependent on pulse duration. In summary, similarly to light, the resetting actions of dark pulses are dependent on both circadian phase and stimulus duration. However, dark pulses appear more complex stimuli, with both photic and nonphotic resetting properties. phase shift; nonphotic; wheel-running; entrainment ALL LIVING ORGANISMS SHOW temporal organization in their physiology and behavior. Endogenous oscillations with a periodicity of ϳ24 h are called circadian rhythms, and in mammals the main circadian pacemaker or clock is contained in the suprachiasmatic nuclei (SCN) of the hypothalamus (24,25). This SCN clock is synchronized (entrained) by recurring external time cues or zeitgebers. Daily variation in environmental light is a potent zeitgeber, and such photic information is relayed directly to the SCN via the monosynaptic retinohypothalamic tract (14

Entrainment and coupling of the hamster suprachiasmatic clock by daily dark pulses

“…Rapid entrainment of the free‐running rhythm was evident when activity offset coincided with the time of dark exposure. Thus, in animals in which the first dark pulse occurred in the subjective midday, a large initial phase advance was observed, as expected from the phase advances induced by dark pulses or nonphotic stimulation (Mrosovsky, 1996; Antle and Mistlberger, 2000; Canal and Piggins, 2006), but the latency of entrainment tooks several days. By contrast, in animals in which the dark pulse coincided with the offset of locomotor activity, a phase delay and a faster entrainment was observed.…”

“…Whereas light resets the SCN clock of animals under constant darkness (DD) conditions (Meijer and Schwartz, 2003), dark pulses can shift the SCN of animals in LL. Dark pulses produce phase advances during the subjective day and early night and phase delays during the late night (Boulos and Rusak, 1982; Ellis et al, 1982; Rosenwasser and Dwyer, 2002; Canal and Piggins, 2006). Moreover, in split hamsters exposed to LL, a dark pulse applied in temporal reference to one of the two split components produces a phase shift of this component, but not of the one in antiphase, accompanied by an unilateral down‐regulation of Per genes expression (Mendoza et al, 2004).…”

Differential firing pattern and response to lighting conditions of rat intergeniculate leaflet neurons projecting to suprachiasmatic nucleus or contralateral intergeniculate leaflet

“…phase advances and delays) during the subjective night (for review see Harrington, 1997 andAllen, 2006). Thus, it is possible that observed increased firing of a subset of IGL neurons projecting to the SCN, is the mechanism of dark pulse-induced phase shift in the daytime described by other researchers (Boulos and Rusak, 1982;Ellis et al, 1982;BarbackaSurowiak, 2000;Rosenwasser, 2002;Canal and Piggins, 2006). A plausible mechanism of the darkness-induced increase in firing of IGL neurons projecting to SCN is relief of these cells of the inhibition caused by enkephalin.…”

Phenobarbital blockade of the preovulatory luteinizing hormone surge: association with phase-advanced circadian clock and altered suprachiasmatic nucleus Period1 gene expression

“…Although vehicle-treated hamsters also exhibited phase advances in their wheel-running rhythms, these phase advances were about half as large as those seen in animals treated with phenobarbital, and the small phase advances were not sufficient to delay the LH surge. These smaller phase advances may have resulted at least in part from the transfer to DD because exposure to a dark "pulse" of at least 3 h duration, or to DD, during the midsubjective day following exposure to constant light can induce a 2-3 h phase shift (2,9). In addition, it is possible that the volume of vehicle injected (10 ml), which was much larger than that typically used in phase-shifting studies, contributed to the phase shift magnitude.…”