Review
The main olfactory system and social learning in mammals

https://doi.org/10.1016/j.bbr.2008.12.021Get rights and content

Abstract

There is increasing evidence for specialised processing of social cues in the brain. This review considers how the main olfactory system of mammals is designed to process social odours and the effects of learning in a social context. It focuses mainly on extensive research carried out on offspring, mate or conspecific learning carried out in sheep and rodents. Detailing the roles of the olfactory bulb and its projections, classical neurotransmitters, nitric oxide, oestrogen and neuropeptides such as oxytocin and vasopressin in mediating plasticity changes in the olfactory system arising from these different social learning contexts. The relative simplicity of the organisation of the olfactory system, the speed and robustness of these forms of social learning together with the similarity in brain regions and neurochemical contributions across the different learning paradigms make them important and useful models for investigating general principles of learning and memory in the brain.

Introduction

Social interactions and bonds are of paramount importance for humans as well as for many other animal species. It is, thus, not surprising that the brain has evolved sophisticated specialisations for the control of social behaviour, recognition, attraction and bonding. For many, it is the complex demands of a social environment which have driven the evolution of the brain and of cognitive functions [38], [39], [40]. A major function of animals’ cognitive abilities being to recognise, manipulate and behave appropriately with respect to socially relevant information. The study of this “social brain” helps us understand the nature and regulation of social interactions between individuals and groups in a particular species. It also allows us to recognise the wide variety of affective and personality disorders where key aspects of normal social behaviour are dysfunctional, making it difficult for such individuals to cope with everyday social demands.

How are social signals perceived and processed? Are these systems exclusive to social stimuli? Different animals rely on different sensory systems to interact with the world. Some sensory systems appear even to have evolved specially for social behaviour. The most notable example of this is the system used for detecting pheromones, the chemosignal compound used for communication between conspecifics (reviewed in [36]). Most social signals, however, are not processed by a specialised sensory system but by common systems adapted for multimodal processing of complex stimuli such as social ones. There are increasing examples of situations where the brain has evolved specialisations for processing key sensory cues for social recognition or where specific aspects of social behaviour are controlled by particular genes [21], [44]. Many studies have now shown that the brain often processes social cues differently than non-social ones. Neuropsychological and neuroimaging studies in humans for example have shown different brain processes for social visual stimuli than for non-social ones. For example, the lateral fusiform gyrus is involved in the recognition of faces and is activated to a greater degree when subjects view faces than other non-face objects [70]. This general region is also involved in recognition of faces in monkeys and sheep [152]. There is also evidence for specialised processing of vocal cues for social communication in humans and other animal species [5]. Finally, while there are obviously a number of different genes involved in different aspects of social behaviour there has been considerable recent interest in those that are involved in social bonds and social recognition memory. In rodents, sheep and humans for example there is also increasing evidence showing that the neuropeptides oxytocin (OT) and vasopressin and their respective receptors play a key role in the control of social recognition memory and in partner and offspring bonding as well as in aspects of social trust and anxiety [45], [56], [60], [88].

Animals in many species rely heavily on the emission and detection of olfactory cues for social recognition; and have developed incredible sensitivity in discriminating between and remembering the chemosignals secreted by conspecifics [167], [168]. This has developed to the point where the inclusion of non-biological odours has little or no effect on learning and recognition of social cues. In a social context, social odours are the prominent cues for social recognition, with artificial odours perhaps adding only motivational or attention value to a social stimulus [67], [126].

The ability to recognise, use and behave according to socially relevant information requires neural systems that process perception of social cues and also those that connect such perception to motivation, emotion and adaptive behaviour. The olfactory bulb is also a simple and easily accessible structure with a well-defined olfactory system and these features make it ideal for studying how sensory cues drive even complex behavioural responses such as social ones. It is, therefore, possible to study the involvement of the different neural substrates at all levels in the system, from the initial sensory detection of odour molecules by the olfactory receptors through to limbic and higher cortical processing.

This review will consider in detail the neural systems and transmitter and hormonal substances involved in the mediation of a number of different examples of olfactory guided social recognition and learning models in mammals and focussing on odours processed by the main olfactory system.

Section snippets

Detection of social chemosignals in mammals by the olfactory system

The mammalian olfactory system has the ability to detect volatile molecules as well as non-volatile ones (peptides and proteins). The nasal cavity of rodents contains two sets of chemosensory neurones located in the vomeronasal organ (VNO) and in the main olfactory epithelium (MOE) (Fig. 1). The MOE neurones project a single axon into a glomerulus and synapse with mitral cells of the main olfactory bulb (MOB) and those in the VNO to mitral cells in the accessory olfactory bulb (AOB). Olfactory

The main olfactory system

Classical anterograde and retrograde tracing studies have provided evidence for two distinct neural networks forming the projections of the vomeronasal and olfactory systems. In the MOS, odours are detected in the MOE by olfactory sensory neurones (OSN) which express one of 1000 different odourant receptor types [19], [99]. The OSN send their axons into the MOB where they synapse with glutamatergic mitral cells which are the output neurones of this region and send projections to different areas

Social olfactory recognition paradigms

Social olfactory recognition involving the MOS has been studied in a number of different animal species although mainly in rodents and ungulates. The behavioural models are based on ethologically important events where learning usually leads to reproductive success or survival. These include maternal recognition of offspring in sheep [79], [116] and social recognition in rats and mice [45], [153]. Offspring recognition ensures the mother will preserve her own genes by limiting maternal

Learning in the main olfactory system

Olfactory recognition memory involves a distributed neural network in the MOS, including secondary and tertiary odour processing regions. The participation of each brain area partly depends on the nature and parameters of the learning task as well as on temporal configurations [73], [114], [127]. There is therefore an anatomical as well as a temporal configuration for the consolidation of memories, similar to other memory models [101].

Valuable information has come from sheep studies on brain

Social olfactory recognition and the MOB

Regardless of the type of task at question, odour learning involves long-lasting neurochemical changes in the olfactory bulb. Similar plasticity changes have been observed in post-partum ewes [80] and in mice following olfactory conditioning [15] social recognition or social transmission of food preference [126], [127]. These changes are caused by a reorganisation of information processing in the OB. The MOB has a simple structure formed by three main cell layers; periglomerular, mitral/tufted

Social olfactory learning, gonadal hormones and vaginocervical stimulation

Many behavioural models of social recognition are based on ethologically relevant behaviours occurring in critical periods of reproduction. This suggests sex hormones play a role in social olfactory memory and that somatosensory stimulation, such as of the vagina and cervix during mating or parturition, might also have a facilitatory effect. For the sheep model, memory formation occurs following the post-partum induction of maternal behaviour resulting from vaginocervical stimulation and high

Social recognition and oestrogen receptors

Recent studies have focussed on establishing the role of oestrogen in neural plasticity associated with social recognition through the activation of it's α or β receptors (αER and βER). We have investigated the involvement of both receptors in olfactory learning by studying short- and long-term social recognition in mice lacking functional αER or βER genes (αERKO and βERKO mice respectively). Our findings show that social recognition memories require a functional αER activated by oestrogen.

The OB plays a primary role in odour-guided behaviour

Olfaction in mammals can strongly mediate diverse behaviours from fear responses to predators and aversive behaviour to avoidance/approach toxic/palatable foods, mate preferences and offspring or maternal recognition. Rodents, for example, show avoidance behaviours towards the odours of predators’ and the smell of spoiled food [58], [59], [158]. They can also show attraction behaviours to specific food or conspecific odours [97], [111]. Some of these behaviours are learned and others are

Conclusions

From this review it is clear that many different aspects of social recognition and social learning involve relevant odour cues being processed by the MOS and that while a distributed system of primary, secondary and tertiary processing regions is involved in associated memory formation, plasticity changes within the olfactory bulb and piriform cortex maintain it post-consolidation. The neurotransmitter systems involved in these plasticity changes are the same as those reported in the

References (173)

  • A.P.C. da Costa et al.

    Olfactory memory and maternal behaviour-induced changes in c- fos and zif/268 mRNA expression in the sheep brain

    Brain Res Mol Brain Res

    (1997)
  • R. Dantzer et al.

    Cerebral lateralization of olfactory-mediated affective processes in rats

    Behav Brain Res

    (1990)
  • H.E.W. Day et al.

    The pattern of brain c-fos mRNA induced by a component of fox odor, 2.5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systemic and processive stress characteristics

    Brain Res

    (2004)
  • D.E. Dluzen et al.

    1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (Mptp) disrupts social memory recognition processes in the male-mouse

    Brain Res

    (1993)
  • D.E. Dluzen et al.

    Modulation of olfactory bulb tyrosine hydroxylase and catecholamine transporter mRNA by estrogen

    Mol Brain Res

    (2002)
  • K.M. Dorries et al.

    Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig

    Physiol Behav

    (1995)
  • M. Engelmann et al.

    Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats

    Physiol Behav

    (1995)
  • J.N. Ferguson et al.

    The neuroendocrine basis of social recognition

    Front Neuroendocrinol

    (2002)
  • B.G. Galef et al.

    Transfer of information concerning distant foods: a laboratory investigation of the ‘information-centre’ hypothesis

    Anim Behav

    (1983)
  • B.G.J. Galef et al.

    Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats

    Physiol Behav

    (1988)
  • R. Guevara-Guzman et al.

    Effects of the estrous cycle on olfactory bulb response to vaginocervical stimulation in the rat: results from electrophysiology ans Fos immunocytochemistry experiments

    Brain Res Bull

    (1997)
  • J.T. Haskins et al.

    Action of estrogen and mechanical vaginocervical stimulation on the membrane excitability of hypothalamic and midbrain neurons

    Brain Res Bull

    (1983)
  • A.L.O. Hebb et al.

    Changes in brain cholecystokinin and anxiety-like behavior following exposure of mice to predator odor

    Neuroscience

    (2003)
  • M. Heinrichs et al.

    Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress

    Biol Psychiatry

    (2003)
  • U.W. Huck et al.

    Olfactory discrimination of estrous condition by the male golden hamster

    Behav Neural Biol

    (1989)
  • I. Izquierdo et al.

    Different molecular cascades in different sites of the brain control memory consolidation

    Trends Neurosci

    (2006)
  • B.A. Johnson et al.

    A learned odor evokes an enhanced Fos-like glomerular response in the olfactory-bulb of young-rats

    Brain Res

    (1995)
  • R.E. Johnston et al.

    Individual scent signatures in golden-hamsters—evidence for specialization of function

    Anim Behav

    (1993)
  • M. Keller et al.

    Mapping of brain networks involved in consolidation of lamb recognition memory

    Neuroscience

    (2005)
  • K.M. Kendrick

    Neurobiological correlates of visual and olfactory recognition in sheep

    Behav Process

    (1994)
  • K.M. Kendrick et al.

    Neural control of maternal behaviour and olfactory recognition of offspring

    Brain Res Bull

    (1997)
  • K.M. Kendrick et al.

    Importance of progesterone and estrogen priming for the induction of maternal-behavior by vaginocervical stimulation in sheep—effects of maternal experience

    Physiol Behav

    (1991)
  • K.M. Kendrick et al.

    Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes

    Physiol Behav

    (1991)
  • E.B. Keverne et al.

    Influence of birth and maternal experience on olfactory bulb neurotransmitter release

    Neuroscience

    (1993)
  • A. Larrazolo-Lopez et al.

    Vaginocervical stimulation enhances social recognition memory in rats via oxytocin release in the olfactory bulb

    Neuroscience

    (2008)
  • J.W. Lee et al.

    Vaginocervical stimulation suppresses the expression of c-fos induced by mating in thoracic, lumbar and sacral segments of the female rat

    Neuroscience

    (1996)
  • F. Levy et al.

    Involvement of the main but not the accessory olfactory system in maternal-behavior of primiparous and multiparous ewes

    Physiol Behav

    (1995)
  • B. Malnic et al.

    Combinatorial receptor codes for odors

    Cell

    (1999)
  • L.A. Arbogast et al.

    Progesterone reverses the estradiol-induced decrease in tyrosine-hydroxylase messenger-RNA levels in the arcuate nucleus

    Neuroendocrinology

    (1993)
  • H. Baker

    Dopamine and substance-P are contained in different populations of tufted cells in the Syrian and Chinese-Hamster main olfactory-bulb

    Chem Senses

    (1986)
  • N.J. Bean et al.

    The effect of carbon-disulfide on food-consumption by house mice

    J Wildlife Manage

    (1988)
  • P. Belin

    Voice processing in human and non-human primates

    Philos Trans R Soc Lon B Biol Sci

    (2006)
  • M.J. Blissitt et al.

    Detection of oestrous-related odour in ewe urine by rams

    J Reprod Fertil

    (1994)
  • P.A. Brennan et al.

    Olfactory recognition: a simple memory system

    Science

    (1990)
  • P.A. Brennan et al.

    Mammalian social odours: attraction and individual recognition

    Philos Trans R Soc Lon B Biol Sci

    (2006)
  • P.A. Brennan et al.

    Neural mechanisms of olfactory recognition memory

  • K.D. Broad et al.

    Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus

    Eur J Neurosci

    (1999)
  • K.D. Broad et al.

    Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory

    Eur J Neurosci

    (2002)
  • W.F. Carr et al.

    Olfactory recognition of conspecifics by domestic Norway rats

    J Comp Physiol Psycol

    (1976)
  • E. Choleris et al.

    An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice

    Proc Natl Acad Sci USA

    (2003)
  • Cited by (136)

    View all citing articles on Scopus
    View full text