Neural responses to maternal praise and criticism: Relationship to depression and anxiety symptoms in high-risk adolescent girls

Abstract

Background: The parent-child relationship may be an important factor in the development of adolescent depressive and anxious symptoms. In adults, depressive symptoms relate to increased amygdala and attenuated prefrontal activation to maternal criticism. The current pilot study examined how depressive and anxiety symptoms in a high-risk adolescent population relate to neural responses to maternal feedback. Given previous research relating oxytocin to maternal behavior, we conducted exploratory analyses using oxytocin receptor (OXTR) genotype.

Methods: Eighteen females (ages 12-16) listened to maternal praise, neutral, and critical statements during functional magnetic resonance imaging. Participants completed the Mood and Feelings Questionnaire and the Screen for Child Anxiety Related Emotional Disorders. The OXTR single nucleotide polymorphism, rs53576, was genotyped. Linear mixed models were used to identify symptom or allele (GG, AA/AG) by condition (critical, neutral, praise) interaction effects on brain activation.

Results: Greater symptoms related to greater right amygdala activation for criticism and reduced activation to praise. For left amygdala, greater symptoms related to reduced activation to both conditions. Anxiety symptoms related to differences in superior medial PFC activation patterns. Parental OXTR AA/AG allele related to reduced activation to criticism and greater activation to praise within the right amygdala.

Conclusions: Results support a relationship between anxiety and depressive symptoms and prefrontal-amygdala responses to maternal feedback. The lateralization of amygdala findings suggests separate neural targets for interventions reducing reactivity to negative feedback or increasing salience of positive feedback. Exploratory analyses suggest that parents' OXTR genetic profile influences parent-child interactions and related adolescent brain responses.

Keywords: Amygdala; Maternal behavior; Oxytocin; Parent-child relations; Prefrontal cortex.

Fig. S1

Average percent signal change within the basolateral amygdala regions of interest to each task condition. Statistical results for amygdala percent signal change are described in the main text, including both condition main effects as well as condition by symptom (anxiety, depression) interaction effects. Error bars represent standard error.

Fig. 1

Schematic of task. Participants viewed one of three colored dots signaling a subsequent praise, neutral, or critical comment, followed by a 4–8 second interstimulus interval (white dot), the 7 second comment recording, and a 10–21 second intertrial interval (white dot). A vigilance cue (gray dot) would be shown at some point during the intertrial, which would remain on the screen until a button press or the end of the intertrial interval. Ratings grids were presented during 1/3 of the intertrial intervals.

Fig. 2

Relationships between anxiety symptoms and brain activation to cues and recordings. (A) Percent signal change (PSC) extracted from basolateral amygdala regions of interest. A1 demonstrates the Screen for Child Anxiety Related Emotional Disorders (SCARED) by condition interaction effect for the right amygdala response to cues. A2 and A3 demonstrate the SCARED by condition interaction effect for the right and left amygdala response to recordings. (B) Prefrontal cortex (PFC) and amygdala clusters identified via whole-brain analyses. B1 and B2 demonstrate interaction effects for medial PFC clusters to cues and recordings, respectively. B3 demonstrates interaction effects for left amygdala to recordings.

Fig. 3

Relationships between OXTR alleles and (A) negative ratings of maternal criticism. (B) left amygdala, and (C) right amygdala.