Maternal Sensitivity during Toddlerhood Predicts Amygdala-PFC Functional Connectivity During Early Adolescence

• In Event: 1-181 - Normative Variation in Early Caregiving: Longitudinal Links to Brain Structure and Function

Integrative Statement

Maternal sensitivity during early childhood has lasting influence on cognitive, linguistic and socioemotional functioning (Fraley, Roisman, & Haltigan, 2013). Yet, links between early caregiving and later neural processes have received less empirical attention. This gap is striking given that the attachment behavioral system is posited to serve an evolutionary survival function rooted in the central nervous system. We examined early maternal sensitivity – a key process that fosters child-mother attachment security – as a predictor of emotion-related neural processes in adolescence. Because the amygdala plays a central role in learning about the emotional significance of the environment (LeDoux, 1996; Tottenham, 2012), we focused on amygdala reactivity (indicative of emotional salience and threat detection) and amygdala-PFC connectivity (indicative of regulation of stress).

At 2.5 years, mothers and toddlers (N = 128, 66 girls) participated in a laboratory visit, and a composite of maternal sensitivity was computed from ratings of maternal behavior across play and snack sessions. At 13.5 years (N = 50, 16 girls), adolescents completed a series of functional MRI scans. In two fMRI tasks, adolescents were presented with emotion faces. In a series of path models (controlling for teen age, gender, and maternal education), we tested early maternal sensitivity as a predictor of adolescents’ neural responses to emotion faces.

Task 1. Adolescents labeled strangers’ ambiguous angry and happy faces, choosing one of three emotion labels: happy, neutral, angry. Maternal sensitivity did not predict amygdala reactivity, but negatively predicted amygdala-mPFC connectivity when labeling angry stranger faces (see Figure 1). For adolescents who experienced lower levels of maternal sensitivity as toddlers, they showed less mature (i.e., positive) amygdala-mPFC connectivity, whereas for adolescents who experienced higher levels of maternal sensitivity as toddlers, they showed more typical amygdala-mPFC connectivity (i.e., around 0, see Gee et al., 2013). This effect did not emerge for happy faces.

Task 2. Adolescents also completed an emotion ‘go no-go’ task consisting of stranger and mother angry, happy and neutral facial expressions. Paralleling Task 1 findings, maternal sensitivity did not predict amygdala reactivity, but negatively predicted amygdala-mPFC connectivity to stranger happy faces, stranger angry faces, and mother angry faces (see Figure 2 for mother angry faces). The pattern of associations indicated less mature (i.e., positive) amygdala-mPFC connectivity for adolescents who experienced less sensitive caregiving at age 2.5. Adolescents experiencing higher levels of maternal sensitivity showed lower levels of amygdala-mPFC connectivity, suggesting a more mature regulatory response.This effect did not emerge for mothers' happy faces.

Complementing prior support for the enduring influence of early sensitivity on later behavioral functioning (Fraley et al., 2013), our results yield consistent evidence that maternal sensitivity in early childhood is associated with adolescents’ neural processing of emotional stimuli, especially cues that may signal threat (i.e., angry faces). Further, more sensitive parenting predicts adolescents’ better emotion regulation at the neural level in relation to both mothers and strangers. Findings will be discussed in the context of early child-mother attachment as a biobehavioral safety-regulating system.

Authors

• Nancy McElwain, University of Illinois at Urbana-Champaign
  Presenting Author

• Xi Chen, University of Illinois
  Non-Presenting Author

• Niyantri Ravindran, The Pennsylvania State University
  Non-Presenting Author

• Ethan M. McCormick, University of North Carolina Chapel Hill
  Non-Presenting Author

• Eva H. Telzer, University of North Carolina Chapel Hill
  Non-Presenting Author