Mammalian social odours: attraction and individual recognition

Abstract

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.

In search of the chemical basis for MHC odourtypes

“…Moreover, the olfactory system processes mixtures in complex ways. Human psychophysical studies indicate that mixtures of more than four or five odourants cannot be deconstructed into their components and that these mixtures are highly sensitive to relative potencies of the odourants in the mixture (Livermore & Laing 1996; see also Brennan & Kendrick 2006). Therefore, for complex mixtures, analysis of individual volatiles, based on what the instrumentation and methods find to be the most prominent, is likely to fail to identify the odours as detected by a mammalian olfactory system.…”

Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons

“…W hile in humans the visual system discriminates individuals 1 , mice, as nocturnals, rely on olfactory cues released by bodily secretions in social behaviours such as mate choice, territorial scent marking and aggression [2][3][4][5] . Mice may identify conspecifics by both the main olfactory epithelium as well as the vomeronasal organ (VNO), responding to bodily secretions such as urine.…”

The evolution of pheromonal communication

“…Both the VNO and MOE have recently been shown to respond to certain volatile odours [87] while MOE sensory neurons have also been shown to be activated by involatile peptides which were previously thought to be detected solely through the VNO [78]. These data indicate that the two olfactory systems do not operate in mutually exclusive sensory domains, however the majority of pheromonal effects in mammals are still thought to be mediated via the VNO [11] and it is only the MOE that has both the appropriate morphology and the complexity of sensory receptor to act as a chemosensor for general airborne odours.…”

“…A functional role has been identified for a recently discovered third chemosensory organ, the Grueneberg ganglion, which appears to mediate behavioural responses to alarm pheromones in rodents [9], however the majority of behaviourally-significant chemosignals are detected by either the MOE or VNO. These two sensory organs have their own distinct primary projection targets, connecting to the main olfactory bulb (MOB) and the accessory olfactory bulb (AOB) respectively, which each then connect to different forebrain nuclei comprising the main olfactory system and the vomeronasal system [11]. The MOB sends projections to secondary processing areas including the piriform cortex, the anterior olfactory nucleus and the cortical amygdala, while the AOB has bidirectional connections with the medial amygdala and the bed nucleus of stria terminalis with further output to the ventral hypothalamus [28].…”

“…While these studies show behavioural effects of human semiochemicals, they also arouse considerable controversy given the limited chemosensory array that humans have compared to small-brained mammals. While the VNO appears during development in foetal humans, its main function is the guidance of migrating GnRH neurons in the early brain [11], and it does not appear to persist in the adult human. Furthermore, the critical genes that code for vomeronasal function have undergone widespread inactivation in the human genome.…”