Right Frontoinsular Cortex and Subcortical Activity to Infant Cry Is Associated with Maternal Mental State Talk

J Neurosci. 2015 Sep 16;35(37):12725-32. doi: 10.1523/JNEUROSCI.1286-15.2015.

Abstract

The study objective was to examine neural correlates of a specific component of human caregiving: maternal mental state talk, reflecting a mother's proclivity to attribute mental states and intentionality to her infant. Using a potent, ecologically relevant stimulus of infant cry during fMRI, we tested hypotheses that postpartum neural response to the cry of "own" versus a standard "other" infant in the right frontoinsular cortex (RFIC) and subcortical limbic network would be associated with independent observations of maternal mental state talk. The sample comprised 76 urban-living, low socioeconomic mothers (82% African American) and their 4-month-old infants. Before the fMRI scan, mothers were filmed in face-to-face interaction with their infant, and maternal behaviors were coded by trained researchers unaware of all other information about the participants. The results showed higher functional activity in the RFIC to own versus other infant cry at the group level. In addition, RFIC and bilateral subcortical neural activity (e.g., thalamus, amygdala, hippocampus, putamen) was associated positively with maternal mental state talk but not with more global aspects of observed caregiving. These findings held when accounting for perceptual and contextual covariates, such as maternal felt distress, urge to help, depression severity, and recognition of own infant cry. Our results highlight the need to focus on specific components of caregiving to advance understanding of the maternal brain. Future work will examine the predictive utility of this neural marker for mother-child function.

Significance statement: The current study advances extant literature examining the neural underpinning of early parenting behavior. The findings highlight the special functional importance of the right frontoinsular cortex-thalamic-limbic network in a mother's proclivity to engage in mental state talk with her preverbal infant, a circumscribed aspect of maternal caregiving purported to be a prerequisite of sensitive and responsive caregiving. These associations existed specifically for maternal mentalizing behavior and were not evident for more generic aspects of caregiving in this urban sample of 76 postpartum mothers. Finally, the findings were robust even when controlling for potential demographic, perceptual, and contextual confounds, supporting the notion that these regions constitute an innate, specialized maternal mentalizing network.

Keywords: affective-perceptual empathy; mental state talk; right frontoinsular cortex (RFIC); subcortical limbic region.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adolescent
  • Black or African American / psychology
  • Brain Mapping*
  • Cerebral Cortex / physiology*
  • Crying*
  • Cues
  • Dominance, Cerebral
  • Emotions*
  • Female
  • Frontal Lobe / physiology*
  • Humans
  • Infant
  • Limbic System / physiology
  • Magnetic Resonance Imaging
  • Maternal Behavior / physiology*
  • Models, Neurological
  • Models, Psychological
  • Mother-Child Relations*
  • Mothers / psychology*
  • Observer Variation
  • Pattern Recognition, Physiological
  • Pennsylvania
  • Socioeconomic Factors
  • Theory of Mind*
  • Thinking / physiology*
  • Verbal Behavior / physiology*
  • Young Adult