Differential inter-subject correlation of brain activity when kinship is a variable in moral dilemma

Abstract

Previous behavioural studies have shown that humans act more altruistically towards kin. Whether and how knowledge of genetic relatedness translates into differential neurocognitive evaluation of observed social interactions has remained an open question. Here, we investigated how the human brain is engaged when viewing a moral dilemma between genetic vs. non-genetic sisters. During functional magnetic resonance imaging, a movie was shown, depicting refusal of organ donation between two sisters, with subjects guided to believe the sisters were related either genetically or by adoption. Although 90% of the subjects self-reported that genetic relationship was not relevant, their brain activity told a different story. Comparing correlations of brain activity across all subject pairs between the two viewing conditions, we found significantly stronger inter-subject correlations in insula, cingulate, medial and lateral prefrontal, superior temporal, and superior parietal cortices, when the subjects believed that the sisters were genetically related. Cognitive functions previously associated with these areas include moral and emotional conflict regulation, decision making, and mentalizing, suggesting more similar engagement of such functions when observing refusal of altruism from a genetic sister. Our results show that mere knowledge of a genetic relationship between interacting persons robustly modulates social cognition of the perceiver.

Figure 1

Inter-subject correlation (ISC) of all 30 subjects during the first viewing of the movie. On top row are shown lateral and on bottom row medial surfaces of left and right cerebral hemispheres. Red-yellow colours indicate areas of significant ISC during movie watching (FDR q < 0.05). Abbreviations: ACC = anterior cingulate cortex, ANG = angular gyrus, CAL = calcarine gyrus, DLPFC = dorsolateral prefrontal cortex, DMPFC = dorsomedial prefrontal cortex, IFG = inferior frontal gyrus, IOG = inferior occipital gyrus, MFG = middle frontal gyrus, MOG = middle occipital gyrus, MTG = middle temporal gyrus, PCC = posterior cingulate cortex, SOG = superior occipital gyrus, SPL = superior parietal lobe, STS/STG = superior temporal sulcus and gyrus, VMPFC = ventromedial prefrontal cortex, a = anterior, d = dorsal, p = posterior, v = ventral.

Figure 2

Differential ISC between the conditions of an assumed genetic and non-genetic sisters and BOLD time series from two exemplary single voxels. (A) Significant differences in brain activity when all subjects watched the movie thinking that the sisters were genetically vs. non-genetically related (FDR q < 0.05, t = 2.1447, for consistent illustration purposes, the figures shows t-values from 3 to 9 and −3 to −9) (N = 30, within subject design). Red-yellow colours indicate areas of significantly higher ISC when the subjects watched the movie as depicting genetically related, as compared to non-genetically related, sisters. Blue colour indicates areas showing significantly higher ISC in the reverse contrast. Abbreviations: ACC = anterior cingulate cortex, CAL = calcarine gyrus, DLPFC = dorsolateral prefrontal cortex, IFG = inferior frontal gyrus, IOG = inferior occipital gyrus, MOG = middle occipital gyrus, PCC = posterior cingulate cortex, SPL = superior parietal lobe, STS/STG = superior temporal sulcus and gyrus, VMPFC = ventromedial prefrontal cortex, a = anterior, d = dorsal, p = posterior, v = ventral. (B) Across subjects averaged BOLD time series of two voxels, one in the area VMPFC that showed significantly higher ISC when the subjects were viewing the sisters as genetic and one time series of a voxel in area V1 (primary visual cortex) that did not show significant between-condition ISC differences. The red line plots the group mean BOLD in the genetic sisters condition and the blue line plots the group mean BOLD in non-genetic sisters condition over the whole length of the movie. Red and blue shades indicate the 25^th and 75^th percentile of the variance.

Figure 3

Experienced emotional valence and arousal as well as physiological parameters when perceiving the sisters in the movie as genetic vs. non-genetic. (A) Shown are dynamic self-ratings of emotional valence and arousal over the whole time course of the movie obtained during re-viewing of the movie after the fMRI sessions when the sisters were viewed as genetically related (red) or non-genetic (blue). The ratings were highly similar and there were no time periods where significant between-condition differences could have been observed. Note that half of the subjects (N = 2 × 15) rated experienced arousal and the rest rated experienced valence after the first fMRI session followed by rating the other emotional dimension after the second fMRI session. Plotted are means for all subjects in the red line for assumed genetic sisters and the blue line for non-genetic sisters condition. Red and blue dashed lines show the 25^th and 75^th percentile of the variance. (B) Eye gaze behavior (N = 29) in the movies when the sisters were perceived as either genetic (right) or non-genetic (left) shown as a violin plot with the red cross depicting the means and green squares the medians. There were no significant differences between the conditions. (C) Breathing and heart rates (N = 30) when the sisters were perceived as either genetic (red) or non-genetic (blue). There were no significant differences between the conditions. Red line plots the condition with assumed genetic sisters and the blue line non-genetic sisters. Red and blue shade show the 25^th and 75^th percentile of the variance.

Figure 4

Having to decide in a simulation between saving one’s sister, friend, and others from crisis regions elicited significant brain activity in the VMPFC, ACC, precuneus, DLPFC, IFG, insula, TPJ and MTG. These activations of subjects (N = 30) were obtained by contrasting the decision phases (from the point of revealing the individuals involved until the decision signaled by the subject’s button press) against non-decision phases (subjects watching the background story depicting the two crisis regions and how the subjects only have resources to save individuals from one of the crisis regions) (FDR q < 0.05, t = 2.0384, for consistent illustration purposes, the figures shows t-values from 3 to 9) Left-lateralized motor and supplementary motor are probably explained by the button press that the subjects performed to announce their decision. Abbreviations: ACC = anterior cingulate cortex, DLPFC = dorsolateral prefrontal cortex, IFG = inferior frontal gyrus, IOG = inferior occipital gyrus, ITG = inferior temporal gyrus, MC = motor cortex, MFC = medial frontal cortex, MOG = middle occipital gyrus, MTG = middle temporal gyrus, PCC = posterior cingulate cortex. SMA = supplementary motor area, SPL = superior parietal lobe, TPJ = temporo-parietal junction,VMPFC = ventromedial prefrontal cortex, a = anterior, d = dorsal, p = posterior, v = ventral.

Figure 5

Activity during moral dilemma decision making as disclosed by GLM analysis (red) and the ISC when the subjects believed in a genetic relationship between the sisters in the movie (blue), along with the overlap of these two maps (violet), as well as the more strict overlap with a conjunction test (yellow); , (FDR q < 0.05, t = 2.0384 for GLM and t = 2.1447 for ISC). Abbreviations: ACC = anterior cingulate cortex, DLPFC = dorsolateral prefrontal cortex, IFG = inferior frontal gyrus, MFC = medial frontal cortex, MOG = middle occipital gyrus, MTG = midddle temporal gyrus, PCC = posterior cingulate cortex. SPL = superior parietal lobe, VMPFC = ventromedial prefrontal cortex, a = anterior, d = dorsal, p = posterior, v = ventral.

Figure 6

Experimental procedure and ISC analysis in the movie watching task. (A) Every subject watched the movie four times, in a 2 × 2 design assuming that the movie characters are either genetic sisters or not genetically related and taking the perspective of the to-be-donor sister Anna or the to-be-recipient sister Kate. The order of all the conditions were counter-balanced. (B) Time series from each voxel from all the fMRI recordings are compared across subjects in pairwise correlations to obtain the mean inter-subject-correlation (ISC).