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Neural correlates of recursive thinking during interpersonal strategic interactions.

ABSTRACT: To navigate the complex social world, individuals need to represent others' mental states to think strategically and predict their next move. Strategic mentalizing can be classified into different levels of theory of mind according to its order of mental state attribution of other people's beliefs, desires, intentions, and so forth. For example, reasoning people's beliefs about simple world facts is the first-order attribution while going further to reason people's beliefs about the minds of others is the second-order attribution. The neural substrates that support such high-order recursive reasoning in strategic interpersonal interactions are still unclear. Here, using a sequential-move interactional game together with functional magnetic resonance imaging (fMRI), we showed that recursive reasoning engaged the frontal-subcortical regions. At the stimulus stage, the ventral striatum was more activated in high-order reasoning as compared with low-order reasoning. At the decision stage, high-order reasoning activated the medial prefrontal cortex (mPFC) and other mentalizing regions. Moreover, functional connectivity between the dorsomedial prefrontal cortex (dmPFC) and the insula/hippocampus was positively correlated with individual differences in high-order social reasoning. This work delineates the neural correlates of high-order recursive thinking in strategic games and highlights the key role of the interplay between mPFC and subcortical regions in advanced social decision-making.

SUBMITTER: Zhen S

PROVIDER: S-EPMC8046141 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectiveRecent findings suggest that diminished processing of positive contextual information about others during interactions may contribute to social impairment in the schizophrenia spectrum. This could be due to general social context processing deficits or specific biases against positive information. We studied the impact of positive and negative social contextual information during social interactions using functional neuroimaging and probed whether these neural mechanisms were associated with real-life social functioning in schizophrenia spectrum disorders.MethodsPatients with a schizophrenia spectrum disorder (N = 23) and controls disorder (N = 25) played three multi-round trust games during functional magnetic resonance imaging scanning, with no, positive and negative information about the counterpart's trustworthiness, while all counterparts were programmed to behave trustworthy. The main outcome variable was the height of the shared amount in the trust game, i.e. investment, representing an indication of trust. The first investment in the game was considered to be basic trust, since no behavioural feedback was given yet. We performed region-of-interest analyses and examined the association with real-life social functioning using the experience sampling method.ResultsSocial contextual information had no effect on patients' first investments, whereas controls made the lowest investment after negative and the highest investments after positive contextual information was provided. Over trials, patients decreased investments, suggesting reduced social reward learning, whereas controls increased investments in response to behavioural feedback in the negative context. Patients engaged the dorsolateral prefrontal cortex less than controls during context presentation and showed reduced activity within the caudate during repayments. In patients, lower investments were associated with more time spent alone and social exclusion and lower caudate activation was marginally significantly associated with higher perceived social exclusion.ConclusionThe failure to adapt trust to positive and negative social contexts suggests that patients have a general insensitivity to prior social information, indicating top-down processing impairments. In addition, patients show reduced sensitivity to social reward, i.e. bottom-up processing deficits. Moreover, lower trust and lower neural activation were related to lower real-life social functioning. Together, these findings indicate that improving trust and social interactions in schizophrenia spectrum needs a multi-faceted approach that targets both mechanisms.

Project description:Recent evidence suggests that our capacities to remember the past and to imagine what might happen in the future largely depend on the same core brain network that includes the middle temporal lobe, the posterior cingulate/retrosplenial cortex, the inferior parietal lobe, the medial prefrontal cortex, and the lateral temporal cortex. However, the extent to which regions of this core brain network are also responsible for our capacity to think about what could have happened in our past, yet did not occur (i.e., episodic counterfactual thinking), is still unknown. The present study examined this issue. Using a variation of the experimental recombination paradigm (Addis, Pan, Vu, Laiser, & Schacter, 2009. Neuropsychologia. 47: 2222-2238), participants were asked both to remember personal past events and to envision alternative outcomes to such events while undergoing functional magnetic resonance imaging. Three sets of analyses were performed on the imaging data in order to investigate two related issues. First, a mean-centered spatiotemporal partial least square (PLS) analysis identified a pattern of brain activity across regions of the core network that was common to episodic memory and episodic counterfactual thinking. Second, a non-rotated PLS analysis identified two different patterns of brain activity for likely and unlikely episodic counterfactual thoughts, with the former showing significant overlap with the set of regions engaged during episodic recollection. Finally, a parametric modulation was conducted to explore the differential engagement of brain regions during counterfactual thinking, revealing that areas such as the parahippocampal gyrus and the right hippocampus were modulated by the subjective likelihood of counterfactual simulations. These results suggest that episodic counterfactual thinking engages regions that form the core brain network, and also that the subjective likelihood of our counterfactual thoughts modulates the engagement of different areas within this set of regions.

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Neural correlates of recursive thinking during interpersonal strategic interactions.

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