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Detection, processing and reinforcement of social cues: regulation by the oxytocin system

Nature Reviews Neuroscience volume 24, pages 761–777 (2023)Cite this article

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Abstract

Many social behaviours are evolutionarily conserved and are essential for the healthy development of an individual. The neuropeptide oxytocin (OXT) is crucial for the fine-tuned regulation of social interactions in mammals. The advent and application of state-of-the-art methodological approaches that allow the activity of neuronal circuits involving OXT to be monitored and functionally manipulated in laboratory mammals have deepened our understanding of the roles of OXT in these behaviours. In this Review, we discuss how OXT promotes the sensory detection and evaluation of social cues, the subsequent approach and display of social behaviour, and the rewarding consequences of social interactions in selected reproductive and non-reproductive social behaviours. Social stressors — such as social isolation, exposure to social defeat or social trauma, and partner loss — are often paralleled by maladaptations of the OXT system, and restoring OXT system functioning can reinstate socio-emotional allostasis. Thus, the OXT system acts as a dynamic mediator of appropriate behavioural adaptations to environmental challenges by enhancing and reinforcing social salience and buffering social stress.

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Fig. 1: Oxytocin projections that regulate social behaviours.
Fig. 2: Oxytocin circuitry involved in the detection and processing of social cues.

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Acknowledgements

The authors thank B. Trainor for critically reading the manuscript. This work was supported by the German Research Foundation (DFG; GRK2174; NE465/34-1; and NE465/37-1).

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  1. Department of Behavioural and Molecular Neurobiology, University of Regensburg, Regensburg, Germany

    Rohit Menon & Inga D. Neumann

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  1. Rohit Menon
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Correspondence to Inga D. Neumann.

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Glossary

Allostasis

Adaptive processes of the body that take place in expectance of, or in response to, external stimuli to maintain physiological and mental stability.

Conspecifics

Individuals belonging to the same species.

Epigenetic modifications

Heritable biochemical modifications of DNA or histones (for example, DNA methylation and histone modifications) that result in long-lasting alteration in gene expression without altering the DNA sequence.

Genetic polymorphisms

Two or more variants of a specific DNA sequence in a population. The most common genetic polymorphisms involve variations at a single nucleotide (single-nucleotide polymorphisms).

G protein-coupled receptor

A cell surface transmembrane receptor that is coupled to proteins that bind guanosine triphosphate or guanosine diphosphate (G proteins). Their stimulation activates isoform-specific (Gi, Gq or Gs) intracellular signalling cascades.

Neuroendocrine cells

Specialized neurons that respond to stimulation by synthesizing and secreting hormones (neurohormones) into the bloodstream (for example, hypothalamic magnocellular oxytocinergic and vasopressinergic neurons).

Neurohypophysis

A brain structure (also called the posterior lobe of the pituitary gland) that is located at the base of the brain, embryologically of neuroectodermal origin and consists of the pars nervosa and the infundibulum. The axons of magnocellular neurons, which are located in the hypothalamus and synthesize the neuropeptides oxytocin and vasopressin, project through the infundibulum, terminate in the pars nervosa and secrete the neurohormones via neurohaemal contacts into the bloodstream.

Neuromodulators

Endogenous substances, often neuropeptides, that are co-released with neurotransmitters and regulate neuronal activity not directly via postsynaptic actions but via modulating neurotransmitter actions.

Neuropeptides

Short-chain polypeptides (for example, oxytocin, vasopressin, orexins and corticotropin-releasing factor) that are synthesized in specialized neurons (neuroendocrine cells) and are released either within the brain as neuromodulators or into the blood as neurohormones. They can be released from various parts of the neuronal membrane (axonal terminals, dendrites and soma) and modulate the activity of target cells via G protein-coupled receptors.

Posttranscriptional modifications

Chemical modifications of the primary mRNA, such as splicing or processing at the 3′ or 5′ end of the mRNA molecule, which result in a mature, functional mRNA.

Reinforcement

The process that supports establishing and enhancing a specific pattern of behaviour.

Social memory

The cognitive and behavioural processes involved in the acquisition, storage and retrieval of social information from individual conspecifics.

Social reward

Pleasurable aspects of interactions with conspecifics.

Transcription factors

Intracellular proteins (such as CREB, MEF-2 or oestrogen receptors) that often represent the endpoints of receptor-coupled intracellular signalling cascades and regulate the expression of their target gene and transcription of DNA into messenger RNA by binding to the DNA, the RNA polymerases or other proteins.

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Menon, R., Neumann, I.D. Detection, processing and reinforcement of social cues: regulation by the oxytocin system. Nat. Rev. Neurosci. 24, 761–777 (2023). https://doi.org/10.1038/s41583-023-00759-w

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