Scheduled Daily Mating Induces Circadian Anticipatory Activity Rhythms in the Male Rat

Abstract

Daily schedules of limited access to food, palatable high calorie snacks, water and salt can induce circadian rhythms of anticipatory locomotor activity in rats and mice. All of these stimuli are rewarding, but whether anticipation can be induced by neural correlates of reward independent of metabolic perturbations associated with manipulations of food and hydration is unclear. Three experiments were conducted to determine whether mating, a non-ingestive behavior that is potently rewarding, can induce circadian anticipatory activity rhythms in male rats provided scheduled daily access to steroid-primed estrous female rats. In Experiment 1, rats anticipated access to estrous females in the mid-light period, but also exhibited post-coital eating and running. In Experiment 2, post-coital eating and running were prevented and only a minority of rats exhibited anticipation. Rats allowed to see and smell estrous females showed no anticipation. In both experiments, all rats exhibited sustained behavioral arousal and multiple mounts and intromissions during every session, but ejaculated only every 2–3 days. In Experiment 3, the rats were given more time with individual females, late at night for 28 days, and then in the midday for 28 days. Ejaculation rates increased and anticipation was robust to night sessions and significant although weaker to day sessions. The anticipation rhythm persisted during 3 days of constant dark without mating. During anticipation of nocturnal mating, the rats exhibited a significant preference for a tube to the mating cage over a tube to a locked cage with mating cage litter. This apparent place preference was absent during anticipation of midday mating, which may reflect a daily rhythm of sexual reward. The results establish mating as a reward stimulus capable of inducing circadian rhythms of anticipatory behavior in the male rat, and reveal a critical role for ejaculation, a modulatory role for time of day, and a potential confound role for uncontrolled food intake.

Circadian Insights into Motivated Behavior

“…When the daily opportunity to mate occurs at night, robust anticipation is observed. Rats also exhibited a strong conditioned place preference to the mating chamber when scheduled mating happens at night (Landry et al 2012). Anticipation is also observed when the scheduled mating occurs during the light phase, a time of day when rats are much less likely to engage in mating (Logan and Leavitt 1992).…”

“…Male rats will anticipate a scheduled daily opportunity to mate (Landry et al 2012). When the daily opportunity to mate occurs at night, robust anticipation is observed.…”

“…As discussed above, the circadian system can anticipate daily opportunities to feed, and the circadian clock is influenced by exercise. When opportunities to engage in these post-coital motivated behaviors (feeding and exercise) were prevented, male rats rarely anticipated the scheduled daytime mating opportunity (Landry et al 2012), suggesting that the observed anticipation of daytime mating may have been related to the exercise and feeding after sex, rather than the mating itself. Similarly, the male rats show no conditioned place preference to the mating chamber when mating is scheduled during the day.…”

Food as circadian time cue for appetitive behavior

“…There certainly are many FEOs, in both the brain and the body, but that does not rule out the possibility that there is a "final common" circadian clock that integrates multiple time cues and ultimately sets the phase and period of anticipatory behavioral rhythms. There is ample evidence that animals can anticipate restricted access to other appetitive stimuli, including highly palatable snacks 88,89 , water 90,91 , salt 92 , reproductively receptive mates 93 , and addictive, psychomotor stimulant drugs 54, [94][95][96] . By contrast, scheduled arousal by sleep deprivation, time-restricted running-wheel access, forced running or swimming does not induce anticipatory activity 97,98 .…”

“…By contrast, scheduled arousal by sleep deprivation, time-restricted running-wheel access, forced running or swimming does not induce anticipatory activity 97,98 . Anticipation of water, sex and drugs has been experimentally separated from effects of these schedules on food intake, ruling out spurious food entrainment 91,93,95 . These appetitive stimuli share with food ingestion the ability to strongly activate DA signaling in neural circuits that mediate reward processing, reinforcement learning and habit formation 99 .…”