A Randomized Controlled Trial of a Parenting Intervention During Infancy Alters Amygdala-Prefrontal Circuitry in Middle Childhood

Abstract

Objective: Early adverse parenting predicts various negative outcomes, including psychopathology and altered development. Animal work suggests that adverse parenting might change amygdala-prefrontal cortex (PFC) circuitry, but work in humans remains correlational. The present study leveraged data from a randomized controlled trial examining the efficacy of an early parenting intervention targeting parental nurturance and sensitivity (Attachment and Biobehavioral Catch-up [ABC]) to test whether early parenting quality causally affects amygdala-PFC connectivity later in life.

Method: Participants (N = 60, mean age = 10.0 years) included 41 high-risk children whose parents were referred by Child Protective Services and randomly assigned to receive either ABC (n = 21) or a control intervention (n = 20) during the children's infancy and a comparison sample of low-risk children (n = 19). Amygdala-PFC connectivity was assessed via functional magnetic resonance imaging while children viewed fearful and neutral faces.

Results: Across facial expressions, ABC produced different changes than the control intervention in amygdala-PFC connectivity in response to faces. The ABC group also exhibited greater responses than the control intervention group to faces in areas classically associated with emotion regulation, including the orbitofrontal cortex and right insula. Mediation analysis suggested that the effect of ABC on PFC activation was mediated by the intervention's effect on amygdala-PFC connectivity.

Conclusion: Results provide preliminary causal evidence for the effect of early parenting intervention on amygdala-PFC connectivity and on PFC responses to face viewing. Findings also highlight amygdala-PFC connectivity as a potential mediator of the effects of early parenting intervention on children's emotion regulation development.

Clinical trial registration information: Intervening Early With Neglected Children; https://clinicaltrials.gov/; NCT02093052.

Diversity & inclusion statement: We worked to ensure sex and gender balance in the recruitment of human participants. We worked to ensure race, ethnic, and/or other types of diversity in the recruitment of human participants. We worked to ensure that the study questionnaires were prepared in an inclusive way. One or more of the authors of this paper self-identifies as a member of one or more historically underrepresented racial and/or ethnic groups in science. One or more of the authors of this paper self-identifies as a member of one or more historically underrepresented sexual and/or gender groups in science. One or more of the authors of this paper received support from a program designed to increase minority representation in science. While citing references scientifically relevant for this work, we also actively worked to promote sex and gender balance in our reference list.

Keywords: amygdala; early adversity; parenting; prefrontal cortex; randomized controlled trial.

Figure 1:. Intervention Effect on Reactivity to Faces

Note: Colored regions indicate statistically significant clusters where experimental intervention (ABC = Attachment and Biobehavioral Catch-up) > control intervention (DEF = Developmental Education for Families) after correction for multiple comparisons. There were no significant clusters where DEF > ABC. Montreal Neurological Institute coordinates X = 5, Y = 18, Z = 4. Error bars indicate +/− 1 SE. Low-risk group parameter estimates are shown in bar graph for comparison. ABC = Attachment and Biobehavioral Catch-up (experimental intervention). DEF = Developmental Education for Families (control intervention). ** p < .01.

Figure 2:. Intervention Effect on Amygdala-Seeded Functional Connectivity to Faces

Note: Colored regions indicate the significant cluster where control intervention (DEF = Developmental Education for Families) > experimental intervention (ABC = Attachment and Biobehavioral Catch-up) after correction for multiple comparisons. There were no significant clusters where ABC > DEF. Montreal Neurological Institute coordinates X = 48, Y = 20, Z = 16. Error bars indicate +/− 1 SE. Low-risk group connectivity estimates are shown in bar graph for comparison. ABC = Attachment and Biobehavioral Catch-up (experimental intervention). DEF = Developmental Education for Families (control intervention). * p < .05. ** p < .01. *** p < .001.

Figure 3:. Mediation Models for Intervention Effects on Amygdala-Seeded Functional Connectivity and Reactivity to Faces

Note: Intervention groups were coded as experimental intervention (ABC = Attachment and Biobehavioral Catch-up) = 1, control intervention (DEF = Developmental Education for Families) = 0; thus, positive estimates for group effects indicate greater scores in the ABC group than in the DEF group. The hypothesized mediation model revealed that 69.9% of ABC’s effect on BOLD reactivity to faces was explained by amygdala-seeded connectivity. In contrast, the alternative model revealed that 35.2% of ABC’s effect on amygdala connectivity was explained by BOLD activation, suggesting that the hypothesized model may better account for the relations among these three variables. * p < .05. ** p < .01. *** p < .001.