Intraspecific Communication Through Chemical Signals in Female Mice: Reinforcing Properties of Involatile Male Sexual Pheromones

Abstract

In rodents, social and reproductive behaviors critically depend on chemical signals, including sexual pheromones that have been suggested (but not demonstrated) to be rewarding. In this work, we analyze this issue by studying the chemoinvestigatory behavior of adult female mice (without experience with male-derived chemicals) toward 1) the synthetic odorant citralva, 2) bedding soiled by different conspecifics (females, males, and castrated males), and 3) volatiles derived from bedding soiled by males and castrated males (confronted in 2-choice tests). We also study whether these chemical signals are able to induce conditioned place preference, a reliable test for rewarding properties of stimuli. The results show that involatile, male-derived chemicals elicit an intense and sustained chemoinvestigation and, more importantly, are the only tested chemical signals that induce conditioned place preference. In contrast, volatile, male-derived chemicals are not significantly chemoinvestigated. Bedding soiled by castrated males induces a transient chemoinvestigation, likely directed to steroid-independent, biologically relevant chemical signals, whereas the intense chemoinvestigation of female-soiled bedding shows a slow habituation. Finally, females did not explore significantly citralva-odorized bedding. The present work constitutes the first demonstration of the unconditioned reinforcing properties of involatile (likely detected by the vomeronasal organ) steroid-dependent chemical signals in mammals.

From sexual attraction to maternal aggression: When pheromones change their behavioural significance

“…Adult females prefer male-to female-derived chemosignals whether presented as an entire anaesthetised animal, a drop of urine or soiled-bedding. Similarly, adult females also prefer intact to castrated male-derived odours (Martinez-Ricos et al, 2007;DiBenedictis et al, 2012).…”

6-Hydroxydopamine lesions of the anteromedial ventral striatum impair opposite-sex urinary odor preference in female mice

“…We hypothesized that the saliency attributed to these odors arises from pheromone-induced activation of the mesolimbic dopamine ‘reward’ system, yet little is known about the neural pathways via which pheromonal stimuli access the mesolimbic dopamine system. Male and female mice will form a conditioned place preference for opposite-sex urinary odors [9,10], suggesting that these odors are rewarding. Additionally, immediate early gene studies have shown that opposite-sex (but not same-sex) conspecific body odorants activate several segments of the brain’s reward circuitry including the mOT (unpublished observations), AcbC, AcbSh, and the ventral tegmental area (VTA) [8,11–12].…”

Airborne molecules released from male mouse urine affect female exploratory behavior

“…A complementary, non-overlapping function has been suggested for volatile molecules and urinary proteins, as the former may act as olfactory flags for the presence of MUP (MucignatCaretta and Caretta, 1999a), while non-volatile chemosignals may act as natural reinforcers that induce conditioned place preference (Martínez-Ricós et al, 2007). In the majority of cases, the two different components of mice chemosignals, volatile, and non-volatile, have been studied independently, so the contribution of each component in the initial phase of attention orienting to the chemical stimuli remains unclear.…”