The effect of criticism on functional brain connectivity and associations with neuroticism

Abstract

Neuroticism is a robust personality trait that constitutes a risk factor for psychopathology, especially anxiety disorders and depression. High neurotic individuals tend to be more self-critical and are overly sensitive to criticism by others. Hence, we used a novel resting-state paradigm to investigate the effect of criticism on functional brain connectivity and associations with neuroticism. Forty-eight participants completed the NEO Personality Inventory Revised (NEO-PI-R) to assess neuroticism. Next, we recorded resting state functional magnetic resonance imaging (rsfMRI) during two sessions. We manipulated the second session before scanning by presenting three standardized critical remarks through headphones, in which the subject was urged to please lie still in the scanner. A seed-based functional connectivity method and subsequent clustering were used to analyse the resting state data. Based on the reviewed literature related to criticism, we selected brain regions associated with self-reflective processing and stress-regulation as regions of interest. The findings showed enhanced functional connectivity between the clustered seed regions and brain areas involved in emotion processing and social cognition during the processing of criticism. Concurrently, functional connectivity was reduced between these clusters and brain structures related to the default mode network and higher-order cognitive control. Furthermore, individuals scoring higher on neuroticism showed altered functional connectivity between the clustered seed regions and brain areas involved in the appraisal, expression and regulation of negative emotions. These results may suggest that the criticized person is attempting to understand the beliefs, perceptions and feelings of the critic in order to facilitate flexible and adaptive social behavior. Furthermore, multiple aspects of emotion processing were found to be affected in individuals scoring higher on neuroticism during the processing of criticism, which may increase their sensitivity to negative social-evaluation.

Figure 1. Four clusters were found using fuzzy c-means clustering for the contrast (criticism > standard): (A) prefrontal cluster (red bars), (B) fronto-temporal cluster (yellow bars), (C) occipito-parietal cluster (green bars) and (D) amygdala/hippocampal cluster (light blue bars).

The seed regions anterior cingulate cortex and SFG(BA10) are depicted in dark blue. On the x-axis, the different seed regions can be found in alphabetical order. On the y-axis, membership degrees are continuously expressed as proximities to a cluster centroid, containing values between 0 and 1. ACC, anterior cingulate cortex; L_Amy, left amygdala; R_Amy, right amygdala; Cun, cuneus; L_Hip, left hippocampus; R_Hip, right hippocampus; L_IFG, left inferior frontal gyrus; L_Ins, left insula; L_SFG, left superior frontal gyrus; L_TP, left temporal pole; PCC/Prec, posterior cingulate cortex/precuneus; SFG(BA10), superior frontal gyrus (BA10); SFG(BA9), superior frontal gyrus (BA9).

Figure 2. Visualization of correlations between the seed regions based on their functional connectivity pattern.

Gephi (0.8.1 – beta) was used to draw the graph. The following colors indicate the cluster to which a specific seed region belongs based on the fuzzy c-means clustering approach: the prefrontal cluster (red), the fronto-temporal cluster (yellow), the occipito-parietal cluster (green) and the amygdala/hippocampal cluster (light blue). The seed regions anterior cingulate cortex and SFG(BA10) are depicted in dark blue. The edges between the nodes have a mixed color. The thickness of the edges represents the strength of the correlation between the seed regions based on their functional connectivity pattern. ACC, anterior cingulate cortex; L_Amy, left amygdala; R_Amy, right amygdala; Cun, cuneus; L_Hip, left hippocampus; R_Hip, right hippocampus; L_IFG, left inferior frontal gyrus; L_Ins, left insula; L_SFG, left superior frontal gyrus; L_TP, left temporal pole; PCC/Prec, posterior cingulate cortex/precuneus; SFG(BA10), superior frontal gyrus (BA10); SFG(BA9), superior frontal gyrus (BA9).

Figure 3. Functional connectivity patterns related to the thirteen seed regions overlayed on a MNI template for the different contrasts: (A) criticism > standard, (B) standard > criticism, (C) criticism > standard, positive correlation with neuroticism and (D) criticism > standard, negative correlation with neuroticism.

Brain regions, showing enhanced functional connectivity to our thirteen seed regions, are depicted in red for seed regions that belong to the prefrontal cluster, in yellow for seed regions that belong to the fronto-temporal cluster, in green for seed regions that belong to the occipito-parietal cluster and in light blue for seed regions that belong to the amygdala/hippocampal cluster. Connectivity results for the seed regions anterior cingulate cortex and SFG(BA10) are depicted in dark blue. Results were corrected on FWE cluster level (k>20) with an initial threshold of p<0.001 uncorrected.