Indiscriminate amygdala response to mothers and strangers after early maternal deprivation

Abstract

Background: In altricial species, maternal stimuli have powerful effects on amygdala development and attachment-related behaviors. In humans, maternal deprivation has been associated with both "indiscriminate friendliness" toward non-caregiving adults and altered amygdala development. We hypothesized that maternal deprivation would be associated with reduced amygdala discrimination between mothers and strangers and increased parent report of indiscriminate friendliness behaviors.

Methods: Sixty-seven youths (33 previously institutionalized; 34 comparison; age-at-scan 4-17 years) participated in a functional magnetic resonance imaging experiment designed to examine amygdala response to mother versus stranger faces. In-scanner behavior was measured. Indiscriminate friendliness was assessed with parental report.

Results: Comparison youth showed an amygdala response that clearly discriminated mother versus stranger stimuli. Previously institutionalized youths, by contrast, exhibited reduced amygdala discrimination between mothers and strangers. Reduced amygdala differentiation correlated with greater reports of indiscriminate friendliness. These effects correlated with age-at-adoption, with later adoptions being associated with reduced amygdala discrimination and more indiscriminate friendliness.

Conclusions: Our results suggest that early maternal deprivation is associated with reduced amygdala discrimination between mothers and strangers, and reduced amygdala discrimination was associated with greater reports of indiscriminate friendliness. Moreover, these effects increased with age-at-adoption. These data suggest that the amygdala, in part, is associated with indiscriminate friendliness and that there might be a dose-response relationship between institutional rearing and indiscriminate friendliness.

Keywords: Affective salience; amygdala development; attachment; indiscriminate friendliness; institutional rearing; maternal deprivation.

Figure 1

Older age-at-adoption was associated with higher parent report of indiscriminate friendliness (adjusted for IQ and age-at-scan). Pearson correlation (r=0.37, p<0.05). Missing IF data N=11 from Comparison group and N=4 from PI group. Total N=40.

Figure 2

A) Whole-brain LME analysis revealed a Group × Stimulus Type interaction (F=4.003, p<0.05, small-volume-corrected): left amygdala ROI (peak [-27 -3 -19]; k=47. B) Unlike the Comp group, who showed greater amygdala signal for mother than stranger stimuli, the PI group showed equivalent signal across stimuli (controlling for age-at-adoption, age-at-scan, and IQ). Stars indicate post hoctests: Mother vs. Stranger – Comp: **p<0.001, PI: p>0.05; Comp vs. PI – Mother: p>0.05, *Stranger: p<0.05.

Figure 3

Amygdala habituation. Comparison youth exhibited a greater decrease in amygdala signal to facial stimuli over the course of the scan session relative to PI youth.

Figure 4

Older age-at-adoption in PI group was associated with less typical amygdala discrimination between mother and stranger stimuli. Pearson correlation r=-0.39, p<0.05. PI group N=31.

Figure 5

Association between amygdala discrimination and indiscriminate friendliness. Participants with more attenuated amygdala discrimination between mother and stranger stimuli tended to exhibit more indiscriminate behaviors as reported by parents (r=-0.28, p<0.05; controlling for IQ, age-at-scan, and age-at-adoption). Missing IF data N=11 from Comparison group and N=4 from PI group. Total N=40.