Viewing Ambiguous Social Interactions Increases Functional Connectivity between Frontal and Temporal Nodes of the Social Brain

Abstract

Social behaviour is coordinated by a network of brain regions, including those involved in the perception of social stimuli and those involved in complex functions like inferring perceptual and mental states and controlling social interactions. The properties and function of many of these regions in isolation is relatively well-understood, but less is known about how these regions interact whilst processing dynamic social interactions. To investigate whether the functional connectivity between brain regions is modulated by social context, we collected functional MRI (fMRI) data from male monkeys (Macaca mulatta) viewing videos of social interactions labelled as "affiliative", "aggressive", or "ambiguous". We show activation related to the perception of social interactions along both banks of the superior temporal sulcus, parietal cortex, medial and lateral frontal cortex, and the caudate nucleus. Within this network, we show that fronto-temporal functional connectivity is significantly modulated by social context. Crucially, we link the observation of specific behaviours to changes in functional connectivity within our network. Viewing aggressive behaviour was associated with a limited increase in temporo-temporal and a weak increase in cingulate-temporal connectivity. By contrast, viewing interactions where the outcome was uncertain was associated with a pronounced increase in temporo-temporal, and cingulate-temporal functional connectivity.We hypothesise that this widespread network synchronisation occurs when cingulate and temporal areas coordinate their activity when more difficult social inferences are being made.

Why the cognitive “fountain of youth” may be upstream: Pathways to dementia risk and resilience through social connectedness

“…The cognitive enrichment provided by social bridging may shape brain health directly, as shown in Figure 1, by triggering gene expression and catalyzing functional connectivity and neuronal growth, including brain repair. [19][20][21][22] These effects of social bridging on the brain are consistent with recent studies indicating that greater network complexity, measured as irregular contact with a diversity of social roles, frequent interactions with friends (but not family members), and less densely connected networks are associated with healthy brain volume and connectivity, and better cognitive functioning in older adults. [23][24][25][26][27][28] Social bridging may also indirectly affect trajectories of cognitive decline through an accumulation of cognitive reserve (see Figure 1).…”

Behavioral context affects social signal representations within single primate prefrontal cortex neurons

“…Communication is social behavior for which signal processing is one component, rather than a system in which a signaling processing system forms the base on top of which behaviors are built. The current study focused solely on PFC but there are reasons to think that the effects of social context on primate neocortical function are more widespread (Ainsworth et al, 2021;Cléry et al, 2021;Sliwa and Freiwald, 2017). Indeed, merely the presence of conspecifics can affect primate decision-making (Chang et al, 2013;Chang et al, 2011), while simply watching conspecific social interactions as a third-party observer has been shown to change the response properties of classically identified face cells to be driven by a myriad of social factors (McMahon et al, 2015).…”

Fine-scale dynamics of functional connectivity in the face processing network during movie watching

“…In addition to the PPC, we observed multiple visual connections to the mPFC and the IFG, regions implicated in the dynamic processing of faces [42][43][44] and the processing of familiar faces 45,46 . In the context of connectivity rather than regional activations, functional connectivity between visual 47 or temporal 48 cortices and the prefrontal cortex is related to the processing of degraded or ambiguous faces or social visual stimuli. Moreover, differences in activations of these frontal face regions were found in Autism Spectrum Disorder (ASD) compared to control while observing faces 49,50 .…”