Social Chemosignals Research Articles

Sniffing out social signals

Abstract In most mammals, conspecific chemical com­munication strategies control complex social and sexual behavior. Just a few years ago, our concept of how the olfactory system is orga­nized to ensure faithful transmission of so­cial information built on the rather simplis­tic assumption that two fundamentally dif­ferent classes of stimuli - ‘general’ odors ver­sus ‘pheromones’ - are exclusively detected by either of two sensory structures: the main olfactory epithelium or the vomeronasal or­gan. A number of exciting recent findings, however, revealed a much more complex and functionally diverse organizational struc­ture of the sense of smell. At least four ana­tomically segregated olfactory subsystems, some remarkably heterogeneous in their cel­lular composition, detect distinct, but partial­ly overlapping populations of sensory stimuli. Discerning how subsystem-specific receptor architectures and signaling pathways orches­trate the coding logic of social chemosignals, will ultimately shed new light on the neuro­physiological basis of social behavior.

Fear-Related Chemosignals Modulate Recognition of Fear in Ambiguous Facial Expressions

Integrating emotional cues from different senses is critical for adaptive behavior. Much of the evidence on cross-modal perception of emotions has come from studies of vision and audition. This research has shown that an emotion signaled by one sense modulates how the same emotion is perceived in another sense, especially when the input to the latter sense is ambiguous. We tested whether olfaction causes similar sensory modulation of emotion perception. In two experiments, the chemosignal of fearful sweat biased women toward interpreting ambiguous expressions as more fearful, but had no effect when the facial emotion was more discernible. Our findings provide direct behavioral evidence that social chemosignals can communicate emotions and demonstrate that fear-related chemosignals modulate humans' visual emotion perception in an emotion-specific way--an effect that has been hitherto unsuspected.

Homeostatic Control of Sensory Output in Basal Vomeronasal Neurons: Activity-Dependent Expression ofEther-à-Go-Go-Related Gene Potassium Channels

Conspecific chemosensory communication controls a broad range of social and sexual behaviors. In most mammals, social chemosignals are predominantly detected by sensory neurons of a specialized olfactory subsystem, the vomeronasal organ (VNO). The behavioral relevance of social chemosignaling puts high demands on the accuracy and dynamic range of the underlying transduction mechanisms. However, the physiological concepts implemented to ensure faithful transmission of social information remain widely unknown. Here, we show that sensory neurons in the basal layer of the mouse VNO dynamically control their input-output relationship by activity-dependent regulation of K(+) channel gene expression. Using large-scale expression profiling, immunochemistry, and electrophysiology, we provide molecular and functional evidence for a role of ether-à-go-go-related gene (ERG) K(+) channels as key determinants of cellular excitability. Our findings indicate that an increase in ERG channel expression extends the dynamic range of the stimulus-response function in basal vomeronasal sensory neurons. This novel mechanism of homeostatic plasticity in the periphery of the accessory olfactory system is ideally suited to adjust VNO neurons to a target output range in a layer-specific and use-dependent manner.

Mammalian social odours: attraction and individual recognition

Mammalian social systems rely on signals passed between individuals conveying information including sex, reproductive status, individual identity, ownership, competitive ability and health status. Many of these signals take the form of complex mixtures of molecules sensed by chemosensory systems and have important influences on a variety of behaviours that are vital for reproductive success, such as parent-offspring attachment, mate choice and territorial marking. This article aims to review the nature of these chemosensory cues and the neural pathways mediating their physiological and behavioural effects. Despite the complexities of mammalian societies, there are instances where single molecules can act as classical pheromones attracting interest and approach behaviour. Chemosignals with relatively high volatility can be used to signal at a distance and are sensed by the main olfactory system. Most mammals also possess a vomeronasal system, which is specialized to detect relatively non-volatile chemosensory cues following direct contact. Single attractant molecules are sensed by highly specific receptors using a labelled line pathway. These act alongside more complex mixtures of signals that are required to signal individual identity. There are multiple sources of such individuality chemosignals, based on the highly polymorphic genes of the major histocompatibility complex (MHC) or lipocalins such as the mouse major urinary proteins. The individual profile of volatile components that make up an individual odour signature can be sensed by the main olfactory system, as the pattern of activity across an array of broadly tuned receptor types. In addition, the vomeronasal system can respond highly selectively to non-volatile peptide ligands associated with the MHC, acting at the V2r class of vomeronasal receptor. The ability to recognize individuals or their genetic relatedness plays an important role in mammalian social behaviour. Thus robust systems for olfactory learning and recognition of chemosensory individuality have evolved, often associated with major life events, such as mating, parturition or neonatal development. These forms of learning share common features, such as increased noradrenaline evoked by somatosensory stimulation, which results in neural changes at the level of the olfactory bulb. In the main olfactory bulb, these changes are likely to refine the pattern of activity in response to the learned odour, enhancing its discrimination from those of similar odours. In the accessory olfactory bulb, memory formation is hypothesized to involve a selective inhibition, which disrupts the transmission of the learned chemosignal from the mating male. Information from the main olfactory and vomeronasal systems is integrated at the level of the corticomedial amygdala, which forms the most important pathway by which social odours mediate their behavioural and physiological effects. Recent evidence suggests that this region may also play an important role in the learning and recognition of social chemosignals.

Parallel processing of social signals by the mammalian main and accessory olfactory systems.

The mammalian olfactory system has evolved complex mechanisms to detect a vast range of molecular cues. In rodents, the olfactory system comprises several distinct subsystems. Current interest has focused on the exact role that each of these subsystems plays in detecting molecular information and regulating chemosensory-dependent behaviors. Here, we summarize recent results showing that the mouse main and accessory olfactory systems detect, at least in part, overlapping sets of social chemosignals. These findings give rise to a model that involves parallel processing of the same molecular cues in both systems. Together with previous work, this model will lead to a better understanding of the general organization of chemical communication in mammals and give a new direction for future experiments.

A putative social chemosignal elicits faster cortical responses than perceptually similar odorants

Social chemosignals, so-called pheromones, have recently attracted much attention in that effects on women's psychophysiology and cortical processing have been reported. We here tested the hypothesis that the human brain would process a putative social chemosignal, the endogenous steroid androstadienone, faster than other odorants with perceptually matched intensity and hedonic characteristics. Chemosensory event-related potentials (ERP) were recorded in healthy women. ERP analyses indicate that androstadienone was processed significantly faster than the control odorants. Androstadienone elicited shorter latencies for all recorded ERP components but most so for the late positivity. This finding indicates that androstadienone is processed differently than other related odorants, suggesting the possibility of a specific neuronal subsystem to the main olfactory pathway akin to the one previously reported in Old-world monkeys and emotional visual stimuli in humans.

Endocrine changes in male stumptailed macaques ( Macaca arctoides) as a response to odor stimulation with vaginal secretions

In mammalian species, social chemosignals are important in modulating endocrine reproductive functions. In nonhuman primates, previous studies have described a high frequency of mounting behavior by females in the follicular and periovulatory phases of the menstrual cycle. Stumptailed macaque females do not signal receptivity by means of sexual swellings, as do others macaques, therefore providing a good model in which to study chemical signaling of reproductive status. We exposed anesthetized stumptailed males to vaginal secretions of either late follicular or menses phase or to saline solution to determine the endocrine changes promoting male sexual behavior. In males exposed to follicular secretions, plasma testosterone concentrations were sustained up to 120 min after exposure. Such an effect was not observed in animals exposed to menses or saline odor sources. A luteinizing hormone surge, occurring 30 minutes after exposure to late follicular phase secretion swabs, preceded this sustained testosterone effect. The fact that late follicular scents induce sustained testosterone concentrations provides support to the idea that stumptailed males draw information concerning female reproductive status from the female's vaginal odor.

Social chemosignals from breastfeeding women increase sexual motivation

Human pheromones, a type of social chemosignal, modulate endocrine function by regulating the timing of ovulation. In animals, pheromones not only regulate ovulation but also female reproductive motivation and behavior. There is no extant evidence that humans produce social chemosignals that affect human sexual motivation or reproductive behavior as occurs in other mammals. Here, we demonstrate that natural compounds collected from lactating women and their breastfeeding infants increased the sexual motivation of other women, measured as sexual desire and fantasies. Moreover, the manifestation of increased sexual motivation was different in women with a regular sexual partner. Those with a partner experienced enhanced sexual desire, whereas those without one had more sexual fantasies. These results are consistent with previous pheromonal effects on endocrine function, and warrant further study of these social chemosignals as candidates for pheromonal processes, including their effects on other aspects of motivation and behavior.

Social chemosignals in five Belontiidae (Pisces) species.

Approach behaviors toward conspecific chemical stimuli of the opposite sex were examined in five Belontiidae species: Betta splendens, Macropodus opercularis, Colisa labiosa, C. lalia, and Trichogaster trichopterus. Approach was measured by (a) preference for section 1 of a three-section tank, which contained a vertical tube that introduced the stimulus water, and (b) occupancy of the tube. Experiments 1A and 1B showed that (a) approach behaviors were displayed by the isolated male Betta only to ripe-female stimulus water, (b) group-housed males of the remaining four species were not attracted to female-conditioned water, and (c) socially isolated males of these four species preferred section 1 during presentation of either ripe- or nonripe-female-inhabited water but occupied the tube only during exposure to ripe-female-conditioned water. The findings of Experiment 2A were that (a) the female Betta, regarless of physiological state, showed approach behaviors to male-inhabited water and (b) only ripe females of the remaining species indicated a preference for section 1 during male-water exposure but performed no tube entries. Results of Experiment 2B indicated that social isolation of the females, especially ripe females, facilitated their approach behaviors.