Photoperiodic and Temporal Influences on Chemosensory Induction of Brain Fos Expression in Female Prairie Voles

Prairie voles (Microtus ochrogaster) typically stop breeding during winter. Male prairie voles respond to winter day lengths with gonadal regression, whereas female voles are relatively unresponsive to photoperiod. Unlike commonly studied laboratory rodents, female prairie voles do not exhibit spontaneous oestrous cycles. Instead, females are induced into oestrus by chemosensory cues from conspecific male urine. The present study investigated the interaction among day length, chemosensory cues and the initial brain responses during oestrus induction in female voles. A single drop of male conspecific urine, saline or skimmed milk was applied to the nares of female prairie voles housed for 9 weeks in either long (LD 16 : 8 h) or short (LD 8 : 16 h) days. Animals were killed 0.5, 1, 2 or 24 h after chemosensory treatment and their brains were processed for Fos immunocytochemistry. Body mass and ovarian fat pad mass were higher, but uterine and ovarian mass were lower, in short-day compared to long-day females. Regardless of photoperiod, Fos- immunoreactivity increased in the granule layer of the accessory olfactory bulb (AOB), the supraoptic nucleus and bed nucleus of the stria terminalis (BNST) (anterior medial) in females treated with male urine compared to the two control groups. Fos staining intensified in the AOB, medial and posterocortical medial amygdala and BNST (posterior ventral), 1 h and 2 h after urine treatment. In the medial preoptic area, anterior and lateral hypothalamus, and ventromedial nucleus of the hypothalamus, Fos-immunoreactivity was elevated in females 2 h after receiving urine. Overall, long-day females displayed higher Fos expression in response to urine than females maintained in short days. These results identify a putative neural circuitry of oestrus induction in this species, and provide an approximate time line of activation in the brain circuit responsible for oestrus induction in prairie voles. Seasonal breeders use day length as a proximal cue to indicate seasons and thus coordinate reproduction with food availability, warm temperatures and rainfall (1, 2). Small mammals that inhabit nontropical latitudes often limit reproduction to spring and early summer to optimize reproductive success. This pattern is observed among prairie voles (Microtus ochrogaster), small, short-lived, socially monogamous rodents that inhabit the grasslands of the midwestern USA (3). In the laboratory, simulated winter day lengths (photoperiods) inhibit reproductive function in prairie voles (4). Although the majority of prairie voles are seasonal breeders, there are reports of photoperiod nonresponsive phenotypes that allow breeding to occur at suboptimal times (5). Unlike commonly studied laboratory rodents, such as rats or mice, female prairie voles do not display spontaneous oestrous cycles. Instead, female prairie voles rely on chemosensory signals from adult, conspecific males to induce them into oestrus. Oestrus induction of female prairie voles requires an intact vomeronasal system (VNS) (6‐10). The nonvolatile oestrus-inducing chemo