Hippocampal contributions to the processing of social emotions

Abstract

Inducing and experiencing emotions about others' mental and physical circumstances is thought to involve self-relevant processing and personal memories of similar experiences. The hippocampus is important for self-referential processing during recall and prospection; however, its contributions during social emotions have not been systematically investigated. We use event-related averaging and Granger causal connectivity mapping to investigate hippocampal contributions during the processing of varieties of admiration and compassion pertaining to protagonists' mental versus physical circumstances [admiration for virtue (AV) versus for skill; compassion for social/psychological pain (CSP) versus for physical pain]. Data were collected using a multistep emotion-induction paradigm that included psychosocial interviews, BOLD fMRI, and simultaneous psychophysiological recording. Given that mnemonic demands were equivalent among conditions, we tested whether: (1) the hippocampi would be recruited more strongly and for a longer duration during the processing of AV and CSP; and (2) connectivity between the hippocampi and cortical systems involved in visceral somatosensation/emotional feeling, social cognitive, and self-related processing would be more extensive during AV and CSP. Results elucidate the hippocampus' facilitative role in inducing and sustaining appropriate emotional reactions, the importance of self-related processing during social emotions, and corroborate the conception that varieties of emotional processing pertaining to others' mental and physical situations engage at least partially distinct neural mechanisms.

Figure 1

Event‐related averages for the time courses of admiration, compassion, and control in the hippocampus in voxels activated for emotions relative to control, with standard errors. Units are percent change in BOLD signal and time in seconds; time courses are not corrected for hemodynamic delay. The volume of interest is displayed in pink. Conditions: AV (green): admiration for virtue; CSP (blue): compassion for social pain; AS (yellow): admiration for skill; CPP (red): compassion for physical pain; C (gray): control. Note the rapid rise and sustained activation not only for AV (green) but also for CSP (blue).

Figure 2

Granger causality maps depicting connectivity of the right hippocampus during admiration for virtue (A) and compassion for social pain (B). fMRI data are from 13 subjects, displayed on the brain of one subject. Talairach x coordinate of each sagittal slice is annotated. Images are thresholded using the false discovery rate statistic, q(FDR) < 0.01. Green indicates influence “toward” the hippocampus; blue indicates influence “from” the hippocampus. Note the extensive connectivity from the insula (in) associated with AV; note also the switch in direction of influence between the hippocampus and anterior cingulate (ac) for AV versus CSP. GCM results for the left hippocampus are described in the text. Retrosplenial cortex (rs); precuneus (pr); posterior cingulate cortex (pc); temporal‐parietal junction (tpj); superior temporal gyrus (stg); superior temporal sulcus (sts).

Figure 3

Schematic depicting the overall pattern of results obtained by the GCM for the AV and CSP conditions. The figure's arrows depict the direction of functional connectivity between the hippocampi and the cortical areas implicated in emotional feeling, social cognition, and self‐related processing.