Odor Is a Time Cue for Circadian Behavior

Abstract

Many physiological and behavioral processes such as sleep and wakefulness, hormone secretion, and olfactory sensitivity exhibit a 24-h rhythmicity that persists in constant conditions with a period close to (circa) 24 h. These circadian rhythms are driven by a network of endogenous clocks residing in various tissues, including the olfactory system, and are synchronized to the outside world by environmental time cues such as light, temperature, and food. In addition to having these well-known zeitgebers of circadian clocks, most environments consist of a multitude of odors that report, for example, the availability of food or the presence of predators--and often, they do so in a time-of-day-dependent manner. Considering the evolutionary significance of odors for various fitness-related behaviors such as mate choice, predator avoidance, and foraging strategies, we asked whether odors--similar to light, temperature, or food--might act as a circadian time cue able to influence circadian locomotor behavior in mammals. Administering individual air flow, periodically saturated with an artificial odor mix, to running wheel-equipped mouse cages, we found that rhythmic odor administrations significantly lengthened the period of circadian activity rhythms. Additionally, odor cues led to partial reemergence of circadian locomotor rhythmicity in suprachiasmatic nuclei (SCN)-lesioned mice, suggesting that the SCN as the central circadian pacemaker are not immediately required for odor-mediated effects on circadian behavior. However, odor-based modulation of circadian behavior did not occur in clock mutant (cry1(-/-) /cry2(-/-)) mice, indicating an odor-mediated mechanism that involves extra-SCN canonical clocks, such as the olfactory clock itself. Our results indicate not only that odor stimuli can act as a circadian time cue modulating circadian behavior but also that odor effects are even more pronounced in the absence of the SCN but nevertheless require the presence of a functional canonical clock.

Maternal Olfactory Cues Synchronize the Circadian System of Artificially Raised Newborn Rabbits

“…In adult rodents, these signals affected the expression of daily patterns of body temperature and wheel-running activity [47,48]. Olfactory cues can also modulate the photic and non-photic entrainment of activity in adult rats [49,50].…”

Temporal behaviour profiles of Mus musculus in nature are affected by population activity

“…Olfaction is the most important sensory modality in mice [1] and plays a key role in social signalling among mice and is the main factor used to recognise individual conspecifics [22,23,30,31,37]. Despite degradation of the residual scents, mice can detect olfactory signals for at least 72 h [24], and can determine the number of conspecifics by their scent [29].…”

“…Olfaction can also influence fear related time-stamp memory in mice [48]. In another rodent, Octogon degus, olfactory stimuli are necessary for social entrainment of circadian rhythms [1,20,25,33]. Thus, olfaction is a putative mechanism by which mice can estimate population density.…”

Daily oscillation of odorant detection in rat olfactory epithelium

“…Three hypotheses could be formed: (i) OE responsiveness variations are independent from the OB, (ii) the OB, which can be entrained by the SCN, drives functional changes in the OE throughout the day or (iii) OE sensitivity fluctuations may lead to a rhythm in OB activity. Interestingly, periodicity in environmental odorant levels has been recently identified as a potential zeitgeber (Abraham et al ., ). This could be exploited to test some of the above hypotheses.…”