Affective and cooperative social interactions modulate effective connectivity within and between the mirror and mentalizing systems

Abstract

Decoding the meaning of others' actions, a crucial step for social cognition, involves different neural mechanisms. While the "mirror" and "mentalizing" systems have been associated with, respectively, the processing of biological actions versus more abstract information, their respective contribution to intention understanding is debated. Processing social interactions seems to recruit both neural systems, with a different weight depending on cues emphasizing either shared action goals or shared mental states. We have previously shown that observing cooperative and affective social interactions elicits stronger activity in key nodes of, respectively, the mirror (left posterior superior temporal sulcus (pSTS), superior parietal cortex (SPL), and ventral/dorsal premotor cortex (vPMC/dPMC)) and mentalizing (ventromedial prefrontal cortex (vmPFC)) systems. To unveil their causal organization, we investigated the effective connectivity underlying the observation of human social interactions expressing increasing cooperativity (involving left pSTS, SPL, and vPMC) versus affectivity (vmPFC) via dynamic causal modeling in 36 healthy human subjects. We found strong evidence for a model including the pSTS and vPMC as input nodes for the observed interactions. The extrinsic connectivity of this model undergoes oppositely valenced modulations, with cooperativity promoting positive modulations of connectivity between pSTS and both SPL (forward) and vPMC (mainly backward), and affectivity promoting reciprocal positive modulations of connectivity between pSTS and vmPFC (mainly backward). Alongside fMRI data, such divergent effective connectivity suggests that different dimensions underlying the processing of social interactions recruit distinct, although strongly interconnected, neural pathways associated with, respectively, the bottom-up visuomotor processing of motor intentions, and the top-down attribution of affective/mental states.

Neural processing of social interaction: Coordinate‐based meta‐analytic evidence from human neuroimaging studies

“…Common activations to the two networks encompassed the posterior middle temporal cortex and pSTS bilaterally, alongside the right premotor cortex (Figure ). As previously discussed, the common involvement of areas associated with representing action meaning (Caspers et al, ; Molenberghs et al, ) might reflect the visuomotor decoding of shared motor goals in social interactions (Arioli, Perani, et al, ).…”

“…The reverse comparison highlighted the posterior middle temporal cortex and pSTS bilaterally (Figure ), likely underpinning the deeper visuomotor analyses required by processing joint, compared with individual, actions. While the outcome of such analyses might provide the mentalizing network with sensorimotor information supporting and constraining inferential processes of shared intention understanding (Arioli, Perani, et al, ; Catmur, ), these results seem to provide limited evidence for “exclusively social” areas, exceeding the contribution of action observation and mentalizing networks, in the human brain.…”

“…Mentalizing and processing interactions were associated with consistent common activations in the dorsomedial prefrontal cortex and posterior cingulate cortex, alongside the TPJ bilaterally (Figure ). While all these areas have been associated with inferences on others' mental states (van Overwalle, ; Van Overwalle & Baetens, ), Sliwa and Freiwald's () data from the monkey brain strongly suggest a role of these regions, and particularly the dorsomedial prefrontal cortex, in decoding shared social intentions over and beyond the visuomotor analyses associated with the action observation network (Arioli, Perani, et al, ; Iacoboni et al, ; Van Overwalle & Baetens, ).…”

“…We first expected to replicate previous meta‐analytic evidence on the role of the mirror/action observation (Caspers et al, ; Molenberghs et al, ) and mentalizing (Bzdok et al, ; Molenberghs, Johnson, Henry, & Mattingley, ; Schurz, Radua, Aichhorn, Richlan, & Perner, ; van Veluw & Chance, ) networks in processing others' actions versus mental states, respectively. Based on our previous evidence (Arioli, Perani, et al, ), we additionally predicted an involvement of both networks in processing interactions, that is, to observe overlapping and specific brain regions between a “social interaction network” and both the action observation and mentalizing networks.…”

“…Considerable evidence on the neural processing of individual actions has supported a functional segregation between the complementary roles of the action observation and mentalizing networks, driven by, respectively, (a) biological actions versus verbal/abstract information; (b) implicit versus explicit tasks; and (c) processing “what” and “how” a person is doing (behavioral states) versus “why” (mental states) (Chiavarino, & Humphreys, ; Spunt, Kemmerer, & Adolphs, ; Spunt & Lieberman, , ). However, this segregation conflicts with their joint activation when processing social interactions , regardless of stimuli type (Arioli et al, ; Centelles, Assaiante, Nazarian, Anton, & Schmitz, ; Iacoboni et al, ; Kujala, Carlson, & Hari, ). Their concurrent engagement might reflect the greater complexity of understanding interactions, which, compared with individual actions, would require both the recognition of joint actions, and a representation of their multiple actors' mental states (Catmur, ).…”