Exposure to Criticism Modulates Left but Not Right Amygdala Functional Connectivity in Healthy Adolescents: Individual Influences of Perceived and Self-Criticism

Abstract

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.

Threatening Beliefs About Self and Others Moderate the Association Between Psychoticism and Psychological Distress

“…People may feel controlled by others' demands and expectations and be preoccupied with concerns about appearing inadequate and making mistakes (Hewitt et al, 2017). Apprehending others' perceptions of the self as critical or judgmental can hyperactivate the perception of negative emotions with defensive functions (e.g., fear, anxiety) and hypoactivate the capacity to regulate and mentalize these very emotions (Bonduelle et al, 2021;Kim et al, 2020;Petrocchi and Cheli, 2019). Socially prescribed perfectionism is associated with higher levels of psychopathology and psychological distress in both clinical and nonclinical samples (Jahromi et al, 2012;Smith et al, 2018aSmith et al, , 2018b.…”

“…Self-critical people tend to perceive interpersonal experiences in a way that focuses on personal inadequacies and shame and to see others as judgmental (Gilbert et al, 2006). When coupled with a tendency for social cognitive distortion, self-criticism may activate threat responses, fueling distress and diminishing the capacity for self-soothing (Bonduelle et al, 2021; Cheli et al, 2021; Gilbert and Mascaro, 2017; Gumley et al, 2010; Petrocchi and Cheli, 2019). From an evolutionary point of view, self-criticism is not maladaptive per se, but may be considered a distinctive and potentially threatening process for individuals functioning within our hyperaffiliative species.…”

Individual differences and relationship contexts in the perception and response to criticism: an emotion and family systems perspective

“…On the other hand, vACC and vmPFC activity are more consistently observed during implicit regulation (Etkin et al, 2010;Quirk et al, 2006;Sotres-Bayon & Quirk, 2010). A recent study also found that after criticism, functional connectivity between the left amygdala with brain regions related to sustained emotional processingspecifically, the left putamen, left mediofrontal orbital cortex, left precuneus and right precentral gyrusincreases (Bonduelle et al, 2021). Increased functional connectivity between the amygdala and the left putamen occurs after inducing stress, which indicates a shift towards more habitual behaviour under stress (Chang & Yu, 2018).…”

“…In addition, functional connectivity between regions were also found to be associated with perceived criticism. In the study by Bonduelle et al (2021), perceived criticism scores were correlated with the increase in functional connectivity between the left amygdala and the left superior parietal cortex and the left precuneus. The left superior parietal cortex also shows functional connections with areas involved in emotion regulation (Kohn et al, 2014) whereas the left precuneus shows increased activation during self-referential processing (Molnar-Szakacs et al, 2013) and ruminative thinking (Burkhouse et al, 2017).…”