The neural basis of human social values: evidence from functional MRI - PubMed (original) (raw)

The neural basis of human social values: evidence from functional MRI

Roland Zahn et al. Cereb Cortex. 2009 Feb.

Abstract

Social values are composed of social concepts (e.g., "generosity") and context-dependent moral sentiments (e.g., "pride"). The neural basis of this intricate cognitive architecture has not been investigated thus far. Here, we used functional magnetic resonance imaging while subjects imagined their own actions toward another person (self-agency) which either conformed or were counter to a social value and were associated with pride or guilt, respectively. Imagined actions of another person toward the subjects (other-agency) in accordance with or counter to a value were associated with gratitude or indignation/anger. As hypothesized, superior anterior temporal lobe (aTL) activity increased with conceptual detail in all conditions. During self-agency, activity in the anterior ventromedial prefrontal cortex correlated with pride and guilt, whereas activity in the subgenual cingulate solely correlated with guilt. In contrast, indignation/anger activated lateral orbitofrontal-insular cortices. Pride and gratitude additionally evoked mesolimbic and basal forebrain activations. Our results demonstrate that social values emerge from coactivation of stable abstract social conceptual representations in the superior aTL and context-dependent moral sentiments encoded in fronto-mesolimbic regions. This neural architecture may provide the basis of our ability to communicate about the meaning of social values across cultural contexts without limiting our flexibility to adapt their emotional interpretation.

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Figures

Figure 1.

Figure 1.

The partial effects for each condition-specific moral sentiment compared with Fixation are displayed (see also Materials and Methods and

Supplementary Table 1

). These are inclusively masked by 2 contrasts: 1) comparing the condition-specific moral sentiment (e.g., pride during POS_S-AG) versus the condition with opposite valence and same agency role (e.g., guilt during NEG_S-AG). 2) comparing versus the condition with opposite agency role and same valence (e.g., gratitude during POS_O-AG). This applies to all depictions of whole brain analyses. Additional a priori ROI analyses were carried out on the simple contrasts versus fixation without applying inclusive masking and all reported regions survived FWE-corrected P = 0.05 over a priori ROIs. All images are displayed at an uncorrected P = 0.005, 4 voxels. Consistent group effects for pride: (a) whole brain, (b) VTA ROI analysis, (c) effect of individual differences for pride, whole brain, (d) individual difference effect for gratitude, whole brain, (e) individual difference effect for guilt, overlay of ventromedial PFC, lateral OFC, basal ganglia, and septum ROIs. (f) Individual difference effect for guilt, ventromedial PFC ROI, masked by contrasts versus pride and indignation/anger. (g) Consistent group effect for indignation/anger, overlay of lateral OFC and insula ROIs. (h) Consistent group effect for indignation/anger, whole brain (see

Supplementary Materials

and Methods on definition of ROIs).

Figure 2.

Figure 2.

(a) Partial effect of descriptiveness of social behavior common across all conditions: right superior aTL (BA22, x = 54, y = 0, z = −3; T = 4.53; FWE-corrected P over a priori ROI = 0.008) and right superior mid-posterior temporal gyrus (BA22, x = 57, y = −18, z = 6; T = 4.6; FWE-corrected P over a priori ROI = 0.008). (b) The same analysis (as in a) inclusively masked by the descriptiveness of social behavior effect in Zahn et al. (2007) within the aTL ROI in right superior aTL (BA22, x = 60, y = −3, z = −3; T = 4.18; FWE-corrected P over a priori mask = 0.005). Activations are displayed at uncorrected P = 0.001, 5 voxels.

Figure 3.

Figure 3.

(a) Regression coefficients for subject-specific moral sentiment frequency covariate effects and standard errors in septum and subgenual cingulate (BA32) peak voxels. Scatter plot for _Z_-transformed fMRI effects for (b) pride in the septum and (c) guilt in the subgenual cingulate. There was a significant interaction of condition and effect of subject-specific moral sentiment covariates on _Z_-transformed fMRI effects within the septum (peak coordinate from

Supplementary Table 1

, univariate ANOVA, SPSS14, outliers _Z_-score outside ±2.5 excluded): _F_107,7 = 3.18, P = 0.03. There was also a significant main effect of the moral sentiment covariate on the septal signal strength _F_114,1 = 4.61, P = 0.03. Unadjusted correlations for septal activity with pride for POS_S-AG: R(29) = 0.46, P = 0.01 (trend for gratitude: R(29) = 0.35, P = 0.06, negative trend for indignation/anger: R(28) = −0.34, P = 0.08, no significant correlations with guilt: R(29) = 0.22, P = 0.25). There was a significant interaction of condition with the moral sentiment covariate effect on the signal within the subgenual PFC: _F_112,3 = 2.63, P = 0.05. Subgenual PFC × NEG_S-AG_guilt: R(28) = 0.66, P < 0.0001 (no significant correlations with other moral sentiments: _P_ > 0.30). There was a significant correlation of gratitude with hypothalamic activity (R = 0.43, P = 0.02). However, when adjusting the correlation for the effects of the other conditions, the overall ANOVA shows no significant effect of condition for the strength of correlation between moral sentiment covariates and hypothalamic activation and also no interaction of condition and moral sentiment covariates (at P = 0.05). Thus the effects in the hypothalamus were not robust enough to survive adjustment on the secondary data analysis.

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