Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

• Published in: Genes, brain and behavior Vol. 21; no. 3; pp. e12781 - n/a
• Main Authors: Prior, Nora H., Bentz, Ehren J., Ophir, Alexander G.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01-03-2022; John Wiley & Sons, Inc
• Subjects: Animals; autism; birdsong; call; Chemoreception; Communication; DNA-Binding Proteins; dopamine; female song; Information processing; Neural networks; Neurobiology; nonapeptides; Pair Bond; pair‐bond maintenance; Perception; Review; Sensation; Sensory evaluation; Sensory integration; Sensory perception; Social Behavior; social behavior network; social decision‐making network; Social interaction; Social interactions; song control system; call; nonapeptides; social decision-making network; pair-bond maintenance; social behavior network; female song; song control system; dopamine; autism; birdsong
• ISSN: 1601-1848; 1601-183X
• DOI: 10.1111/gbb.12781

Organisms filter the complexity of natural stimuli through their individual sensory and perceptual systems. Such perceptual filtering is particularly important for social stimuli. A shared “social umwelt” allows individuals to respond appropriately to the expected diversity of cues and signals during social interactions. In this way, the behavioral and neurobiological mechanisms of sociality and social bonding cannot be disentangled from perceptual mechanisms and sensory processing. While a degree of embeddedness between social and sensory processes is clear, our dominant theoretical frameworks favor treating the social and sensory processes as distinct. An integrated social‐sensory framework has the potential to greatly expand our understanding of the mechanisms underlying individual variation in social bonding and sociality more broadly. Here we leverage what is known about sensory processing and pair bonding in two common study systems with significant species differences in their umwelt (rodent chemosensation and avian acoustic communication). We primarily highlight that (1) communication is essential for pair bond formation and maintenance, (2) the neural circuits underlying perception, communication and social bonding are integrated, and (3) candidate neuromodulatory mechanisms that regulate pair bonding also impact communication and perception. Finally, we propose approaches and frameworks that more fully integrate sensory processing, communication, and social bonding across levels of analysis: behavioral, neurobiological, and genomic. This perspective raises two key questions: (1) how is social bonding shaped by differences in sensory processing?, and (2) to what extent is sensory processing and the saliency of signals shaped by social interactions and emerging relationships?
Defining the brain networks that support social communication and behavior has tremendous value for elucidating brain function and supporting broad translational applications for human mental health and well‐being. The foundations and trajectories of prairie vole and zebra finch neurobiological research are quite different, but together these two well‐studied species offer complementary perspectives on what an integrated social‐sensory communication circuit might look like. We believe that integrating the social behavior/decision making network with brain regions responsible for chemosensory and auditory processing provides a platform for such research. Designing experiments that focus on how social experience modulates perception, sensory processing, and communication promise to be particularly powerful for clarifying how social bonding produces lasting impacts on brain and behavior.