The Neural Bases of Social Intention Understanding: The Role of Interaction Goals

<div><p>Decoding others' intentions is a crucial aspect of social cognition. Neuroimaging studies suggest that inferring <em>immediate</em> goals engages the neural system for action understanding (i.e. mirror system), while the decoding of <em>long-term</em> intentions requires the system subserving the attribution of mental states (i.e. mentalizing). A controversial issue, stimulated by recent inconsistent results, concerns whether the two systems are concurrently vs. exclusively involved in intention understanding. This issue is particularly relevant in the case of social interactions, whose processing has been mostly, but not uncontroversially, associated with the mentalizing system. We tested the alternative hypothesis that the relative contribution of the two systems in intention understanding may also depend on the shared <em>goal</em> of interacting agents. To this purpose, 27 participants observed social interactions differing in their cooperative vs. affective shared goal during functional-Magnetic-Resonance-Imaging. The processing of both types of interactions activated the right temporo-parietal junction involved in mentalizing on action goals. Additionally, whole-brain and regions-of-interest analyses showed that the action understanding system (inferior prefrontal-parietal cortex) was more strongly activated by cooperative interactions, while the mentalizing-proper system (medial prefrontal cortex) was more strongly engaged by affective interactions. These differences were modulated by individual differences in empathizing. Both systems can thus be involved in understanding social intentions, with a relative weighting depending on the specific shared goal of the interaction.</p> </div

Neural bases of observing affective social interactions.

<p>The cerebral regions that were significantly activated during the observation of affective social interactions compared with landscape pictures (p<0.05 corrected for multiple comparisons).</p><p>K = cluster-extension in number of voxels (2×2×2 mm³), H = Hemisphere, L = Left, R = Right, BA = Brodmann area.</p

Direct comparisons: affective vs. cooperative social interactions.

<p>The cerebral regions that were more strongly activated during the observation of affective than cooperative social interactions (p<0.05 corrected for multiple comparisons).</p><p>K = cluster-extension in number of voxels (2×2×2 mm³), H = Hemisphere, L = Left, R = Right, BA = Brodmann area.</p

Direct comparisons: cooperative vs. affective social interactions.

<p>The cerebral regions that were more strongly activated during the observation of cooperative than affective social interactions (p<0.05 corrected for multiple comparisons).</p><p>K = cluster-extension in number of voxels (2×2×2 mm³), H = Hemisphere, L = Left, R = Right, BA = Brodmann area, IFG = Inferior Frontal Gyrus, SPL = Superior Parietal Lobule. An asterisk in the “Anatomical region” column denotes assignment by the Anatomy-Toolbox <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-Eickhoff1" target="_blank">[48]</a>.</p

Regions-Of-Interest (ROIs) associated with social cognition.

<p>Graphical description of the regions involved in “action understanding” (i.e. mirror system; blue), “mentalizing on action goals” (green) and “Theory-of-Mind” (i.e. mentalizing proper, e.g. on false beliefs; violet) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-VanOverwalle2" target="_blank">[15]</a>, along with intention understanding by the mirror system (red) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-Iacoboni1" target="_blank">[9]</a>, according to previously published papers <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-VanOverwalle1" target="_blank">[2]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-Iacoboni1" target="_blank">[9]</a>. The regions were defined as 6-mm-radius spheres centred on the centre-of-mass of several previously reported MNI stereotactic coordinates for the right temporo-parietal-junction (TPJ), right dorsal and ventral premotor cortex (dPMC and vPMC), dorsomedial and ventromedial prefrontal cortex (dmPFC and vmPFC) <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347-VanOverwalle1" target="_blank">[2]</a> (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#s2" target="_blank">Methods</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347.s002" target="_blank">Tables S1</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042347#pone.0042347.s003" target="_blank">S2</a>). A dashed yellow contour highlights the common involvement of the right TPJ in mirror motor resonance (blue), mentalizing on action goal (green) and mentalizing proper (i.e. on false beliefs, ToM; violet). The distance (in mm) from the origin of the MNI coordinate-system located in the anterior commissure is reported below each section.</p

Interaction between gender and picture-type.

<p>The cerebral regions that were more strongly activated in females than males when observing cooperative (vs. affective) social interactions (p<0.001 uncorrected for multiple comparisons).</p><p>K = cluster-extension in number of voxels (2×2×2 mm³), H = Hemisphere, L = Left, R = Right, BA = Brodmann area.</p

The effect of interaction goal on the neural processing of human social interactions.

<p>The brain regions activated during the observation of either cooperative (top left) or affective (top right) social interactions, as well as those more strongly activated by cooperative vs. affective (bottom left) or affective vs. cooperative (bottom right) social interactions (p<0.05 FWE corrected for multiple comparisons). The brain regions that were commonly activated while observing cooperative and affective interactions (p<0.001 uncorrected for multiple comparisons) are shown in the centre of the figure. Functional activations have been overlaid on an average-brain from individual subjects' T1-weighted images. The distance (in mm) from the origin of the MNI coordinate-system located in the anterior commissure is reported below each section.</p

The effect of gender and empathic aptitude on the neural processing of human social interactions.

<p>Top: the brain regions that were more strongly activated in females than males when observing cooperative vs. affective interactions (2×2 interaction-analysis), overlaid on an average-brain from individual subjects' T1-weighted images (p<0.001 uncorrected for multiple comparisons). Bottom: the significant correlation between empathic aptitude and intensity of neural activity (parameter estimates) in the right IFG involved in intention understanding (red sphere) when observing cooperative interactions, and in the vmPFC involved in mentalizing (blue sphere) when observing affective interactions, in female (violet dots) and males (green dots) participants. Both parameter estimates and empathy-scores are represented as z-values in the scatterplots. The distance (in mm) from the origin of the MNI coordinate-system located in the anterior commissure is reported below each section.</p