Structural basis of empathy and the domain general region in the anterior insular cortex

Abstract

Empathy is key for healthy social functioning and individual differences in empathy have strong implications for manifold domains of social behavior. Empathy comprises of emotional and cognitive components and may also be closely linked to sensorimotor processes, which go along with the motivation and behavior to respond compassionately to another person's feelings. There is growing evidence for local plastic change in the structure of the healthy adult human brain in response to environmental demands or intrinsic factors. Here we have investigated changes in brain structure resulting from or predisposing to empathy. Structural MRI data of 101 healthy adult females was analyzed. Empathy in fictitious as well as real-life situations was assessed using a validated self-evaluation measure. Furthermore, empathy-related structural effects were also put into the context of a functional map of the anterior insular cortex (AIC) determined by activation likelihood estimate (ALE) meta-analysis of previous functional imaging studies. We found that gray matter (GM) density in the left dorsal AIC correlates with empathy and that this area overlaps with the domain general region (DGR) of the anterior insula that is situated in-between functional systems involved in emotion-cognition, pain, and motor tasks as determined by our meta-analysis. Thus, we propose that this insular region where we find structural differences depending on individual empathy may play a crucial role in modulating the efficiency of neural integration underlying emotional, cognitive, and sensorimotor information which is essential for global empathy.

Keywords: auditory perception; emotion; individual differences; language; pain; sensorimotor integration; social neuroscience; voxel-based morphometry.

Figure 1

(A) Significant correlation in the left dorsal anterior insular cortex (AIC) between individual empathy scores in 101 healthy females and individual cortical gray values (p < 0.001). Axial slice at the (MNI) x/y/z coordinate [−30, 7.5, 4.5] (global, maximal correlation). T-values are color-coded. (B) Correlation of individual gray matter density (arbitrary units) and empathy scores at the peak coordinates from (A). We report these correlations for descriptive purposes. Our conclusions are entirely based on the findings as shown in (A) because one has to keep in mind that the strength of correlation at peak coordinates as shown in (B) may overestimate the true effect (Vul et al., 2009).

Figure 2

(A) Activation likelihood estimate (ALE) findings in the left insula and the MNI z coordinates (on the y-axis) and y coordinates (on the x-axis) related to the physical pain investigated with fMRI (red), emotion (yellow), empathy for pain (purple), hand (turquoise), and foot movement (green). The solid gray line indicates the mean outline of the left sagittal insula and the dashed gray line the central sulcus of the insula dividing the insula in an anterior and posterior part (see methods for more details). Importantly, studies on emotion in healthy individuals entering this ALE analysis did not include insula-coordinates which were related to the measurement of peripheral physiological changes. In a recent meta-analysis responses related to peripheral physiological changes resulting from emotional experiences were located in the ventral anterior insular cortex (Mutschler et al., 2009). Pain-related maximal ALE were found in the posterior insula (left) and in the dorsal anterior insula [left and right, see reference Mutschler et al. (2012) for more details]. Response peaks related to task-set processing based on conjoint analysis of data from 10 different fMRI tasks are indicated by red dashed circles [that is the approximate position of the domain-general region (DGR) of the insular cortex described in reference Dosenbach et al. (2006)], and peaks related to social norm violation (Sanfey et al., 2003), meta-analytically defined, supra-modal aesthetic appraisal (Brown et al., 2011), and sense of agency of hand movements (Farrer and Frith, 2002) by black squares, triangles, and star, respectively. Sense of agency of hand movements overlapped with sensorimotor processing. (B) Empathy-related voxel-based morphometric (VBM) findings in the left insula (indicated by black squares) overlapped with empathy and emotion and sensorimotor-related ALE, but also with the DGR. Blue dots represent empathy for pain-related coordinates from reference Singer et al. (2004).