An insular view of the social decision-making network

Abstract

Social animals must detect, evaluate and respond to the emotional states of other individuals in their group. A constellation of gestures, vocalizations, and chemosignals enable animals to convey affect and arousal to others in nuanced, multisensory ways. Observers integrate social information with environmental and internal factors to select behavioral responses to others via a process call social decision-making. The Social Decision Making Network (SDMN) is a system of brain structures and neurochemicals that are conserved across species (mammals, reptiles, amphibians, birds) that are the proximal mediators of most social behaviors. However, how sensory information reaches the SDMN to shape behavioral responses during a social encounter is not well known. Here we review the empirical data that demonstrate the necessity of sensory systems in detecting social stimuli, as well as the anatomical connectivity of sensory systems with each node of the SDMN. We conclude that the insular cortex is positioned to link integrated social sensory cues to this network to produce flexible and appropriate behavioral responses to socioemotional cues.

Keywords: Emotion; Insular cortex; Sensory integration; Social communication; Social decision making.

FIGURE 1. Schematic of insula connectivity with unimodal thalamic relay nuclei, primary sensory areas, and the social decision-making network.

Thalamic nuclei encode and relay sensory information that conveys affect from the external environment to primary sensory areas where sensory information is decoded and assigned meaning. This information is also relayed via parallel projections to the insular cortex, where social cues are contextualized with internal physiology and other factors to produce unique output patterns in insula efferents that influence SDMN network activity and generate flexible behaviors. Few connections exist between thalamic nuclei and SDMN nodes, except for the following: medial geniculate nucleus projects to AH, MeA and PAG; ventroposterior medial nucleus projections to BNST and LS; lateral geniculate nucleus projects to Hipp (orange circles) and, likewise, unimodal cortical connectivity with SDMN is sparse (beige circles; see section 3.1 for anatomical connections) so sensory information must reach the SDMN via other projections. Insular cortex is well-connected with thalamic relay nuclei, primary sensory areas, and most SDMN structures, suggesting IC is positioned to integrate sensory cues to influence SDMN activity and, therefore, contribute to the integration of socioemotional information with social behaviors. Abbreviations: MeA: Medial amygdala; AH: Anterior hypothalamus; VMH: Ventromedial hypothalamus; mPOA: Medial preoptic area; BNST: Bed nucleus stria terminalis; LS: Lateral septum; Hipp: Hippocampus; VTA: Ventral tegmental area; VP: Ventral pallidum; NAc: Nucleus accumbens core; PAG: Periaqueductal grey; BLA: Basolateral amygdala; LGN: Lateral geniculate nucleus; MGN: Medial geniculate nucleus; VPL: ventroposterior lateral nucleus of the thalamus; VPM: ventroposterior medial nucleus of the thalamus.