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.

Figure 1

MHC class I peptide ligands act as vomeronasal chemosignals of MHC identity owing to the binding characteristics of their anchor residues. Both endogenous and foreign proteins are degraded into nine amino acid peptides by the proteosomal degradation pathway. MHC class I proteins are loaded with the subset of peptides possessing anchor residues that specifically bind to their peptide binding groove. When these peptides are released in body secretions they can act as ligands at the V2R class of vomeronasal receptor, in which the peptide binding specificity is determined by the MHC-dependent positions of their anchor residues.

Figure 2

Distinct patterns of glomerular activity in the main olfactory bulb are found in response to urine odours from mice of difference MHC type. (a) The schematic shows the positional relationship between regions of the main olfactory bulb and the two-dimensional contour maps. Average c-fos glomerular activation patterns in the main olfactory bulbs of H-2^d female mice in response to; (b) clean air, (c) H-2^b male urine odour and (d) H-2^k male urine odour. Colour bar to the right of b shows the density of active glomeruli for b–d (number of positive glomeruli per bin). (e) Colour contour map of the difference between H-2^b and H-2^k odour representations assessed by Mann–Whitney U test. Colour bar to the right of e shows the p values. The black border indicates the critical value for the differences to be regarded as significant. Modified with permission from Schaefer et al. (2002). Copyright 2002 by the Society for Neuroscience.

Figure 3

Accessory olfactory bulb mitral cells respond selectively to the strain identity of anaesthetized stimulus animals. Significant excitatory responses are indicated in red and significant inhibitory responses are indicated in green. Non-significant responses are shown in black and hatched boxes indicate stimulus animals that were not tested. Colour scale at the right represents response indices ranging from −2 to 3. Numbers to the left are identifiers of the individual neurons, some of which were excited by specific strain–sex combinations (7.11–2.8), others by animals of both sexes of a single strain (10.9 and 2.5y). Neuron 9.2x was excited by the majority of stimulus animals and did not show strain specificity. Reprinted with permission from Luo et al. (2003). Copyright 2003 AAAS.

Figure 4

Schematic of the major projections of the main olfactory system and the vomeronasal system in the rat. Selected second order connections are shown to highlight the interconnectivity of the two chemosensory pathways at the level of the amygdala and their convergence on outputs to the hypothalamus and BNST (Pitkänen 2000). Abbreviations: ACo, anterior cortical nucleus; AOB, accessory olfactory bulb; AON, anterior olfactory nucleus; BAOT, bed nucleus of the accessory olfactory tract; BNST, bed nucleus of the stria terminalis; ENT, entorhinal cortex; Me, medial nucleus; MOB, main olfactory bulb; MOE, main olfactory epithelium; NLOT, nucleus of the lateral olfactory tract; OT, olfactory tubercle; PIR, piriform cortex; PMCo, posterior medial cortical nucleus; PLCo, posterior lateral cortical nucleus; VNO, vomeronasal organ.