The role of the midcingulate cortex in monitoring others' decisions

Abstract

A plethora of research has implicated the cingulate cortex in the processing of social information (i.e., processing elicited by, about, and directed toward others) and reward-related information that guides decision-making. However, it is often overlooked that there is variability in the cytoarchitectonic properties and anatomical connections across the cingulate cortex, which is indicative of functional variability. Here we review evidence from lesion, single-unit recording and functional imaging studies. Taken together, these support the claim that the processing of information that has the greatest influence on social behavior can be localized to the gyral surface of the midcingulate cortex (MCCg). We propose that the MCCg is engaged when predicting and monitoring the outcomes of decisions during social interactions. In particular, the MCCg processes statistical information that tracks the extent to which the outcomes of decisions meet goals when interacting with others. We provide a novel framework for the computational mechanisms that underpin such social information processing in the MCCg. This framework provides testable hypotheses for the social deficits displayed in autism spectrum disorders and psychopathy.

Keywords: anterior cingulate cortex; autism spectrum disorders (ASD); empathy; midcingulate cortex; prediction error; psychopathy; social cognition; social reward.

Figure 1

The Midcingulate Cortex (MCC). (A) Cytoarchitecture of the MCC taken from Vogt et al. (1995). The areas shaded in green lie in the MCC_s. The areas shaded in red lie on the MCC_g. We argue that this area is engaged when processing information about others' decisions. Specifically we argue that areas 24a' and 24b', which lie on gyral surface of the cingulate cortex, extending on average 22 mm posterior to and 30 mm anterior to the anterior commisure denoted by (*). (B) Lesion site of the MCC_g and ACC_g (red) and the MCC_s and the ACC_s (green) from Rudebeck et al. (2006). The lesions that affected the gyrus caused disruptions to social behavior and disrupted the processing of social stimuli. (C) Subdivisions of the MCC and ACC according resting-state connectivity (Beckmann et al., 2009). Cluster 7 shown in dark red corresponds, broadly, to the MCC_g.

Figure 2

Neuroimaging the MCC. The top panel shows activity in the same portion of the MCC_g in three fMRI studies investigating reward processing during social interactions. (A) Activity in the MCC_g (the cluster in red, MNI coordinate: −6, 12, 26) correlating with the volatility of advice given by a social confederate on a reward-based decision-making task, taken from Behrens et al. (2008). Activity in this cluster correlated with individual differences in the influence that the advice had on the subjects' own decision-making. (B) Activity in the MCC_g [taken from Apps et al. (2013)] signaling a prediction error when the outcome of another's decision was unexpectedly positive (coordinate: 0, 8, 28), but not to the expected or unexpected outcomes of a computer's responses. (C) Activity shown in the MCC_g (coordinate: 4, 22, 20) correlating with the anticipated net-value (benefit-cost) of a reward to be received by another person, but not rewards that will be received one's self [taken from Apps and Ramnani (under review)]. The bottom panel shows the results of resting-state connectivity analysis in Autism Spectrum Disorders by Balsters et al. (in prep). Connectivity between the MCC, cluster 5 shown in red (D), and the pSTS (E) was reduced in ASD compared to control participants.