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Dynamic influences on the neural encoding of social valence

Nature Reviews Neuroscience volume 23, pages 535–550 (2022)Cite this article

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Abstract

Social signals can serve as potent emotional triggers with powerful impacts on processes from cognition to valence processing. How are social signals dynamically and flexibly associated with positive or negative valence? How do our past social experiences and present social standing shape our motivation to seek or avoid social contact? We discuss a model in which social attributes, social history, social memory, social rank and social isolation can flexibly influence valence assignment to social stimuli, termed here as ‘social valence’. We emphasize how the brain encodes each of these four factors and highlight the neural circuits and mechanisms that play a part in the perception of social attributes, social memory and social rank, as well as how these factors affect valence systems associated with social stimuli. We highlight the impact of social isolation, dissecting the neural and behavioural mechanisms that mediate the effects of acute versus prolonged periods of social isolation. Importantly, we discuss conceptual models that may account for the potential shift in valence of social stimuli from positive to negative as the period of isolation extends in time. Collectively, this Review identifies factors that control the formation and attribution of social valence — integrating diverse areas of research and emphasizing their unique contributions to the categorization of social stimuli as positive or negative.

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Fig. 1: Social alignment: a coarse parameterization of interactions between the self and other with positive or negative valence.
Fig. 2: Factors influencing social valence assignment and circuits underlying those factors.
Fig. 3: A model of the temporal effects of social isolation.

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Acknowledgements

K.M.T. is a Howard Hughes Medical Institute (HHMI) Investigator and the Wylie Vale Professor at the Salk Institute for Biological Studies, and this work was supported by funding from Clayton Foundation, Kavli Foundation, Dolby Family Fund, R01-MH115920 (US National Institute of Mental Health (NIMH)), R37-MH102441 (NIMH) and Pioneer Award DP1-AT009925 (US National Center for Complementary and Integrative Health (NCCIH)). M.Z. is supported by K99/R00 MH108734 (NIMH), a Whitehall Foundation Award, a Sloan Fellowship and a Klingenstein-Simons Fellowship Award. N.P.-C. is supported by Burroughs Wellcome Fund and R00-MH124435 (NIMH).

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Authors and Affiliations

  1. Department of Neuroscience, College of Medicine, University of Florida, Gainesville, FL, USA

    Nancy Padilla-Coreano

  2. HHMI-Salk Institute for Biological Studies, La Jolla, CA, USA

    Kay M. Tye

  3. Department of Neurobiology, School of Medicine, University of Utah, Salt Lake City, UT, USA

    Moriel Zelikowsky

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  1. Nancy Padilla-Coreano
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  2. Kay M. Tye
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  3. Moriel Zelikowsky
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N.P.-C., M.Z. and K.M.T. researched data for the article. All authors made substantial contributions to the discussion of the content, wrote the article, and reviewed and edited the article before submission.

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Correspondence to Kay M. Tye.

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Glossary

Sociability

A parameter describing the degree to which an animal seeks social contact or engages in social interactions.

Valence

The degree to which something is pleasurable (positive) or aversive (negative).

Social context

The social aspects related to the environment that an individual is in. This can include social rank and the presence or absence of others, as well any history of social interactions (such as fighting, mating and so on) in that context.

Social rank

The social position of an individual relative to others in a group (for example, social hierarchy).

Social valence

The valence assigned to a social stimulus or agent.

Cooperation

Two or more individuals with common or shared goals.

Competition

Two or more individuals with goals which are incompatible or in conflict.

Social alignment

The degree to which the goals of the self are in cooperation (‘aligned’) versus in competition (‘opposed’) with the goals of the other.

Social history

The collective social experience of an individual. This includes social memories, social rank, isolation history, group size and other related social experiences.

Social attributes

The physical attributes of a social agent including their age, size, rank, resource-holding potential and so on.

Social heuristics

Generalized associations that can facilitate rapid assessment of a social agent.

Brain state synchrony

When the internal brain state of a social agent is synchronized to the brain state of another social agent, such that changes in one produce changes in the other.

Theory of mind

The ability to create a model of another’s mind as distinct from one’s own by inferring their mental state, logic, beliefs and emotions.

Emotional contagion

The phenomenon of individuals mimicking the emotions or emotional behaviours of others.

Social homeostasis model

A conceptual model proposing that there is an optimal quality and/or quantity of social contact, regulated by a detector, control centre and effector system.

Social dominance

The repertoire of behaviours expressed by higher ranking animals including winning during competition and species-specific body poses.

Mixed selectivity

The ability of neurons to respond consistently to multiple, statistically independent variables.

Valence associative learning

Learning the association between two or more stimuli in which one of the stimuli has a positive or negative valence.

Familiarity

The degree to which two individuals know each other.

Engrams

Ensembles of neurons that undergo enduring changes during learning and facilitate memory recall.

Social preference

The preference for social stimuli (as opposed to non-social stimuli) observed in rodents.

Spatial–social memory

Memory of the space in which a social interaction occurred, often indexed by changes in the time spent in that social space.

Rebound social interaction

The increase in social interaction observed immediately after a social deficit.

Social anxiety

The decrease in social interaction and/or social preference observed following a negative social experience (for example, prolonged isolation, social defeat and so on).

Threat responsivity

The degree to which a host of behavioural responses are expressed in response to a threatening, noxious stimulus, including: freezing, darting, activity bursting, flinching, vocalizations and so on.

Homeostatic set point

Within any homeostatic system, there is a control centre that stores a ‘set point’ and computes the difference between the detected input and the optimal set point.

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Padilla-Coreano, N., Tye, K.M. & Zelikowsky, M. Dynamic influences on the neural encoding of social valence. Nat Rev Neurosci 23, 535–550 (2022). https://doi.org/10.1038/s41583-022-00609-1

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