Trends in Cognitive Sciences
ReviewDopaminergic-neuropeptide interactions in the social brain
Introduction
Social interaction in humans is complex, compared with the social relationships between other animal species. The way in which we relate to others involves many disparate neural functions, including representations of internal somatic states, knowledge about the self, social perceptions and interpersonal motivations. All are orchestrated to support normal, skilled social adaptation. Underpinning social responsiveness is a set of skills termed ‘social cognition’. Successful social interactions require us to observe other people's behaviour, to predict the behaviour of others in relation to ourselves [1] and to respond appropriately. As children, we become increasingly aware of our own actions and their impact on the physical and social world. Social understanding, language and imitation are probably learned through neural systems that respond both during our own actions and when we see others behaving in a similar way [2]. The development of social cognition involves the coordinated action of a network of cortical loci, the original components of which were outlined by Brothers [3]. They included the amygdala, orbito-frontal cortex and aspects of the temporal cortex (the temporo-parietal junction, posterior superior temporal sulcus and the temporal poles) to which we now add the medial prefrontal cortex, the adjacent paracingulate cortex and the ‘mirror’ system [4]. We discuss emerging evidence for a range of genetic and hormonal influences on the coordinated functioning of these regions.
Section snippets
Neural circuits of the social brain
The neural interconnectivity of the ‘social brain’ is outlined schematically in Figure 1 and discussed in Box 1. The amygdala is central to the schema because of its role in associating social stimuli (auditory, visual and olfactory) with value [5]. Accordingly, it directs our unconscious responses during social encounters [1] and alerts us to potential threats posed by sensory stimuli (in addition to being aroused by sexual imagery). The reciprocal connections of the amygdala with the primary
OT and AVP
OT and AVP are neuropeptides, differing in structure by just two of nine amino acids. Nonapeptides similar to OT and AVP are found in diverse species, and their relative chemical similarity indicates that they have long been conserved during evolution. Both have widespread receptor-mediated effects on behaviour and physiology [12]. The sex steroids estrogen and androgen, respectively, modulate their synthesis and their receptors (although species-specific differences occur) and thereby
OT
OT is synthesized in the magnocellular neurosecretory cells that are located in the supraoptic and paraventricular nuclei of the hypothalamus, and in the parvocellular neurons of the paraventricular nuclei. Projections from the magnocellular cells of the hypothalamus link to the posterior pituitary, from which OT is released into the general circulation. The parvocellular neurons of the paraventricular nuclei project to the limbic system (hippocampus, amygdala, striatum, hypothalamus and
AVP
AVP is synthesized primarily in the magnocellular cells of the supraoptic and paraventricular nuclei of the hypothalamus [41]. From here, axons project to the posterior pituitary from where it is released into general circulation. It acts primarily as an antidiuretic hormone. There are also several populations of smaller, parvocellular neurons within the paraventricular nuclei, the bed nucleus of the stria terminalis, the medial amygdala and suprachiasmatic nucleus [42] in which synthesis is
Interaction between dopaminergic, OT and AVP systems
Evidence for the importance of interaction between the dopaminergic, OT and AVP systems, exists in several brain areas and at several levels. There is little doubt that, in humans, activity in dopaminergic reward pathways is associated with socially affiliative behaviours, and it is modulated by OT and AVP activity. This modulation does not necessarily imply that the receptors for dopamine, OT and AVP are proximal to one another in the brain. It is possible that interactions between
Conclusions
Underlying social cognition is a coordinated neural network. The normal functioning of that network engages the neuropeptides OT and AVP with activity of dopaminergic receptors in the striatum and the orbitofrontal cortex 63, 69. Together, their actions permit social recognition, trust and a range of socially affiliative behaviours. Sexual dimorphism in aggression, parenting style and pair-bonding reflects differential activity in this system, which is modulated by sex steroids: in males
Acknowledgements
D.H.S. was supported by the Wellcome Trust, the Nancy Lurie Marks Family Foundation, the Simons Foundation and the European Commission (Framework 6) during the preparation of this article. L.G. was supported by the Health Research Board of Ireland and Autism Speaks during the preparation of this article.
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