Sex differences in the neural correlates of affective experience

Abstract

People believe that women are more emotionally intense than men, but the scientific evidence is equivocal. In this study, we tested the novel hypothesis that men and women differ in the neural correlates of affective experience, rather than in the intensity of neural activity, with women being more internally (interoceptively) focused and men being more externally (visually) focused. Adult men (n = 17) and women (n = 17) completed a functional magnetic resonance imaging study while viewing affectively potent images and rating their moment-to-moment feelings of subjective arousal. We found that men and women do not differ overall in their intensity of moment-to-moment affective experiences when viewing evocative images, but instead, as predicted, women showed a greater association between the momentary arousal ratings and neural responses in the anterior insula cortex, which represents bodily sensations, whereas men showed stronger correlations between their momentary arousal ratings and neural responses in the visual cortex. Men also showed enhanced functional connectivity between the dorsal anterior insula cortex and the dorsal anterior cingulate cortex, which constitutes the circuitry involved with regulating shifts of attention to the world. These results demonstrate that the same affective experience is realized differently in different people, such that women's feelings are relatively more self-focused, whereas men's feelings are relatively more world-focused.

Keywords: anterior cingulate; anterior insula; extraceptive; fMRI; interoceptive.

Fig. 1

Momentary emotional experience (ratings of subjective arousal level) measures in men and women. (A) The bar graph shows mean ratings of subjective arousal level when men and women observed all IAPS images, with error bars indicating 1 s.d. Men and women did not differ in the intensity of their subjective experiences of arousal in response to evocative images overall [F(1, 32) = 1.56, P < 0.220, η_p² = 0.047]. Red bar (F), female; blue bar (M), male. (B) The bar graphs show mean ratings of subjective arousal level when men and women observed, each, negative, positive and neutral IAPS images, with error bars indicating 1 s.d. Men and women did not differ in the intensity of their subjective experiences of arousal in response to negative images [T(32) = 0.81, P < 0.0421], although a significant valence (negative, positive and neutral) × sex (male, female) interaction [F(1.7, 53.6) = 5.72, P < 0.008, η_p² = 0.152] indicated that men reported relatively stronger subjective experiences of arousal than women in response to positive [T(32) = 2.34, P < 0.025] and neutral [T(32) = 2.03, P < 0.050] images. Red bar (F), female; blue bar (M), male.

Fig. 2

Sex differences in the association between neural responses and subjective arousal ratings. (A) The two upper left brain maps show the clusters within the insula that have significantly stronger association in women than in men between neural responses and subjective arousal ratings (P < 0.005 for the purpose of illustration). Blue line divides insula into dorsal and ventral sectors. Note that these regions were mostly located in more ventral or mid part of AI, not dorsal AI. The upper right brain map shows the clusters within the left primary visual area (V1) that have significantly stronger association in men than in women between neural responses and subjective arousal ratings (P < 0.005 for the purpose of illustration). The bar graphs below the brain map show parameter estimates of modulation effects of subjective ratings, with error bars indicating one standard error of the mean. Rt, right hemisphere; Lt, left hemisphere; vAI, ventral anterior insula (AI); mAI, mid AI; red bar (F), female; blue bar (M), male. Each coordinate below the graphs indicates the peak MNI coordinate (x, y, z mm) of each cluster. (B) Whole brain analysis of correlation between neural response to all IAPS pictures and subjective arousal rating (parametric modulation analysis) in men compared with women. Stronger correlation in women than men (t range 1.8–4.0 for illustration) is colored in red-yellow, and stronger correlation in men than women is colored in blue-green. Greater anterior insula (AI) extending to middle insula (MI) activation was confirmed in women than in men, whereas men show greater V1 association than women. Additional exploratory results demonstrate that women had greater association with arousal in other affective areas including the amygdala (AMG) extending to parahippocampal cortex than men, whereas men had greater association with arousal in ventrolateral prefrontal cortex (vlPFC) (see Table 1 for complete cluster table).

Fig. 3

Sex differences during task performance in the functional connectivity between insula ROIs and the dACC. (A) Seed ROI locations in the AI for functional connectivity analyses. The circles on the AI surface show 11 spherical ROIs. The coordinates at the center of each sphere are the ones reported in a meta-analysis (Kurth et al., 2010). The green and yellow ROIs are associated with ‘emotion’, and blue ROIs are associated with ‘attention’. In ‘emotion’ coordinates, green ROIs include multimodal integrated regions that might be also activated by the tasks for other different categories (i.e. not ‘specific’ to emotional tasks). On the other hand, yellow ROIs were the regions specific to emotional tasks (Kurth et al., 2010). (B) The upper figures show the ROIs rendered on brain surface maps (to illustrate insula, a part of temporal/frontal/parietal regions is cropped) and the clusters in ACC with a statistically significant sex difference (men vs women) of functional connectivity (during task performance) to the respective anterior insula (AI) ROI labeled with a colored dot. A blue line divides the insula into dorsal and ventral parts. Functional connectivity from each seed ROI [see (A)] to ACC was calculated. The three ROIs in the AI shown on the map were those that showed statistically significant stronger functional connectivity to the dACC in men than in women. Note that these seed regions in the AI were mostly located in the mid or dorsal AI (not ventral AI). The graphs below the brain map show mean functional connectivity (correlation coefficient r) in each sex group, with error bars indicating one standard error of the mean. Rt, right side; Lt, left side; dAI, dorsal AI; mAI, mid AI; red bar (F), female; blue bar (M), male. Each coordinate described below the graph represents center MNI coordinate (x, y, z, mm) at each ROI.

Fig. 4

Functional connectivity from V1 ROIs to other visual areas in each sex group. The figures show maps of functional connectivity (correlation coefficient r, range 0.4–1.0) based on a seed in the left V1 [left figures; MNI coordinate (x, y, z) = (10, 86, 0) mm] and right V1 [right figures; (x, y, z) = (12, 84, 4) mm] in women (upper figures) and men (lower figures). The two seed ROIs were obtained from the parametric modulation analysis from all participants (height and extent threshold at P < 0.05, FDR-corrected), and further restricted to V1 anatomically. Each coordinate in the figure is the center in each right and left V1 ROI. The figures indicate a similar localization of correlation in surrounding visual areas (V2–V5) in men and women. There was no significant difference in V1 functional connectivity between men and women.