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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.

SUBMITTER: Servaas MN

PROVIDER: S-EPMC3724923 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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

Servaas Michelle Nadine MN Riese Harriëtte H Renken Remco Jan RJ Marsman Jan-Bernard Cornelis JB Lambregs Johan J Ormel Johan J Aleman André A

PloS one 20130726 7

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 neurotici ...[more]

PMID: 23922755

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Project description:Background: Frequent exposure to criticism is a known risk factor for various adult psychiatric disorders. Adolescents may be even more vulnerable to (parental) criticism, as their imbalanced brain maturation makes them prone to stronger mood changes and less effective emotional regulation. Identifying which adolescent subgroups are more vulnerable than others could be of great clinical relevance. Perceived criticism (PC) and self-criticism (SC), two related but distinct traits, could well be crucial vulnerability factors. Hypotheses: After exposure to criticism during fMRI scanning, rapid changes in amygdalar functional connectivity (FC) with other brain areas involved in emotion regulation and social cognitive processing will occur. These changes will depend on trait moderators, such as the adolescents' proneness to (a) perceive others as critical of them (PC) or (b) perceive themselves positively or negatively (SC). Methods: Sixty-four healthy 14-17-year-olds were exposed to a series of auditory comments. Changes in mood states were assessed based on the Profile of Mood States (POMS) prior to and after exposure to these segments. Pre- and post-experiment FC of the left and right amygdalae with other brain areas were also measured. Correlates between FC changes and psychometric measures-including the perceived criticism measure (PCM) and self-perception profile for adolescents (SPPA)-were assessed. Results: First, after being criticized, FC increases of the left amygdala seed region with brain areas related to sustained emotional processing were found, but no right amygdalar FC changes. Second, there was a significant positive partial correlation between individual PCM scores and FC changes between the left amygdala seed region and the left precuneus and left superior parietal cortex, both part of the default mode network. Conclusion: Exposure to criticism resulted in a rapid negative mood change accompanied by an increase in FC between the left amygdala and regions known to be involved in sustained emotional processing, but no right amygdalar FC changes. Furthermore, higher PC but not SC was correlated with stronger left amygdalar FC increases with these regions, suggesting an elevated vulnerability for disturbed emotional processing, as observed in mood disorders, in healthy adolescents with higher PCM scores.

Project description:Monitoring one's performance helps detect errors and adapt to prevent future mistakes. However, elevated performance monitoring is associated with increased checking behaviors and perfectionism and is characteristic of multiple psychiatric disorders. Understanding how heightened performance monitoring in early childhood relates to subsequent brain connectivity may elucidate mechanistic risk factors that influence brain and psychiatric outcomes. The aim of this study was to examine the association between performance monitoring in preschool-aged children and functional connectivity during adolescence. In the current prospective longitudinal study, we performed seed-based functional connectivity analysis using a dorsal anterior cingulate cortex (dACC) seed to assess brain-behavior relationships between observationally coded performance monitoring in preschool-aged children and adolescent functional connectivity (n = 79). We also utilized enrichment analysis to investigate network-level connectome-wide associations. Seed-based analysis revealed negative correlations between preschool performance monitoring and adolescent fc between dACC and orbitofrontal and dorsolateral prefrontal cortex while a positive correlation was observed between dACC-occipital cortex connectivity. Enrichment analysis revealed a negative correlation between preschool performance monitoring and connectivity between motor (MOT) - cingulo-opercular (CO) and salience (SN) - Reward (REW) and a positive correlation with MOT-DMN, and cerebellum (CB) - motor connectivity. Elevated performance monitoring in early childhood is associated with functional connectivity during adolescence in regions and networks associated with cognitive control, sensorimotor processing and cortico-striatal-thalamic-cortico (CTSC) aberrations. These regions and networks are implicated in psychiatric disorders characterized by elevated performance monitoring. Findings shed light on a mechanistic risk factor in early childhood with long-term associations with neural functioning.

Project description:Background: The "primacy effect," i.e., increased memory recall for the first items of a series compared to the following items, is reduced in amnestic mild cognitive impairment (aMCI). Memory task-fMRI studies demonstrated that primacy recall is associated with higher activation of the hippocampus and temporo-parietal and frontal cortical regions in healthy subjects. Functional magnetic resonance imaging (fMRI) at resting state revealed that hippocampus functional connectivity (FC) with neocortical brain areas, including regions of the default mode network (DMN), is altered in aMCI. The present study aimed to investigate whether resting state fMRI FC between the hippocampus and cortical brain regions, especially the DMN, is associated with primacy recall performance in aMCI. Methods: A number of 87 aMCI patients underwent resting state fMRI and verbal episodic memory assessment. FC between the left or right hippocampus, respectively, and all other voxels in gray matter was mapped voxel-wise and used in whole-brain regression analyses, testing whether FC values predicted delayed primacy recall score. The delayed primacy score was defined as the number of the first four words recalled on the California Verbal Learning Test. Additionally, a partial least squares (PLS) analysis was performed, using DMN regions as seeds to identify the association of their functional interactions with delayed primacy recall. Results: Voxel-based analyses indicated that delayed primacy recall was mainly (positively) associated with higher FC between the left and right hippocampus. Additionally, significant associations were found for higher FC between the left hippocampus and bilateral temporal cortex, frontal cortical regions, and for higher FC between the right hippocampus and right temporal cortex, right frontal cortical regions, left medial frontal cortex and right amygdala (p < 0.01, uncorr.). PLS analysis revealed positive associations of delayed primacy recall with FC between regions of the DMN, including the left and right hippocampus, as well as middle cingulate cortex and thalamus (p < 0.04). In conclusion, in the light of decreased hippocampus function in aMCI, inter-hemispheric hippocampus FC and hippocampal FC with brain regions predominantly included in the DMN may contribute to residual primacy recall in aMCI.

Dataset Information

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

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

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