The Impact of Caregiving on the Association Between Infant Emotional Behavior and Resting State Neural Network Functional Topology

Abstract

The extent to which neural networks underlying emotional behavior in infancy serve as precursors of later behavioral and emotional problems is unclear. Even less is known about caregiving influences on these early brain-behavior relationships. To study brain-emotional behavior relationships in infants, we examined resting-state functional network metrics and infant emotional behavior in the context of early maternal caregiving. We assessed 46 3-month-old infants and their mothers from a community sample. Infants underwent functional MRI during sleep. Resting-state data were processed using graph theory techniques to examine specific nodal metrics as indicators of network functionality. Infant positive and negative emotional behaviors, and positive, negative and mental-state talk (MST) indices of maternal caregiving were coded independently from filmed interactions. Regression analyses tested associations among nodal metrics and infant emotionality, and the moderating effects of maternal behavior on these relationships. All results were FDR corrected at alpha = 0.05. While relationships between infant emotional behavior or maternal caregiving, and nodal metrics were weak, higher levels of maternal MST strengthened associations between infant positive emotionality and nodal metrics within prefrontal (p < 0.0001), and occipital (p < 0.0001) cortices more generally. Positive and negative aspects of maternal caregiving had little effect. Our findings suggest that maternal MST may play an important role in strengthening links between emotion regulation neural circuitry and early infant positive behavior. They also provide objective neural markers that could inform and monitor caregiving-based interventions designed to improve the health and well-being of vulnerable infants at-risk for behavioral and emotional problems.

Infant social interactions and brain development: A systematic review

“…Participants were predominantly White (n = 34) and educated (n = 33). Only five studies included lower income families ( Hanford et al, 2018 ; Lyons-Ruth et al, 2016 ; Jones et al, 2009 ; Diego et al, 2006 ; Field et al, 2003 ). In addition to studies of the typical population, this review included two studies that compared infants with, and without, an increased familial likelihood of developing autism spectrum disorders (ASD) ( Eggebrecht et al, 2017 ; Elsabbagh et al, 2015 ), and eleven studies investigated depressed mothers, out of which one study ( Diego et al, 2002 ) did not have a control group.…”

“… Global Rating Scale (GRS; Murray et al, 1996 ); Sethna et al, 2017 Extent to which the caregiver expressed positive emotions during the task through her tone of voice and facial expressions. Calkins et al, 2004 Bernier et al, 2016 Kraybill and Bell, 2013 Adapted version of Gartstein et al, 2008 , 2018 Gartstein et al, 2020 Perone and Gartstein, 2019 Positive and negative affect of the caregiver Feldman et al, 2011 St. John et al, 2017 Affectionate touch Combination of deep affectionate touch (firm patting, stroking, massaging with the whole hand) and light affectionate touch (affectionate kissing, caressing, or stroking, grazing, hugging) Adapted version of Touch Scoring Instrument ( Polan and Ward, 1994 ) Hardin et al, 2021 Communication Mind-Mindedness – comments about infant internal states or intentionality Meins et al, 2001 Dégeilh et al, 2018 Custom Hanford et al, 2018 Infant-directed speech Feldman et al, 2011 St. John et al, 2017 ...…”

“… Calkins et al, 2004 Bernier et al, 2016 Kraybill and Bell, 2013 Adapted version of Gartstein et al, 2008 , 2018 Gartstein et al, 2020 Perone and Gartstein, 2019 Positive and negative affect of the caregiver Feldman et al, 2011 St. John et al, 2017 Affectionate touch Combination of deep affectionate touch (firm patting, stroking, massaging with the whole hand) and light affectionate touch (affectionate kissing, caressing, or stroking, grazing, hugging) Adapted version of Touch Scoring Instrument ( Polan and Ward, 1994 ) Hardin et al, 2021 Communication Mind-Mindedness – comments about infant internal states or intentionality Meins et al, 2001 Dégeilh et al, 2018 Custom Hanford et al, 2018 Infant-directed speech Feldman et al, 2011 St. John et al, 2017 Disruptive communication Atypical Maternal Behavior Instrument for Assessment and Classification ( Lyons-Ruth et al, 1999 ) Lyons-Ruth et al, 2016 Directiveness or support for autono...…”

“… Dégeilh et al (2018) 28 Maternal behaviours & resting functional connectivity of brain networks 13, 15 mths Mother: MM (13 mon); support for autonomy (15 mon) 10 yrs fMRI ↑ MM predicted ↑ negative connectivity between DMN (vmPFC, right angular gyrus) and SN (AI);↑Autonomy support predicted ↑ negative connectivity between DMN (AI) and SN (dACC, bilateral AI). Hanford et al (2018) 46 Effect of infant affect & maternal behaviours on neural networks 3 mths Infant: affect Mother: warmth, hostility, intrusiveness, involvement, sensitivity, MM 3 mths fMRI ↑ maternal MM linked to ↑positive associations between infant positive emotionality & nodal metrics within prefrontal & occipital cortices, bilateral insula; and ↑ negative associations between infant positive emotionality & nodal metrics within R supramarginal gyrus and L STS. ↑ positive caregiving linked to ↓ negative relationship between infant positive emotionality & L OFC;↓ negative caregiving linked to↑ relationship between infant negative emotionality & R inferior parietal lobule; Perone and Gartstein (2019) 51 Infant frontal-posterior functional connectivity & caregiver-infant interaction 6–11 mths Mother: responsiveness, emotional tone, reciprocity.…”

Patterns of Infant Amygdala Connectivity Mediate the Impact of High Caregiver Affect on Reducing Infant Smiling: Discovery and Replication

“…25 infants were excluded for incomplete scans, excessive motion and/or artifact, and 2 mothers did not complete the postpartum depression scale(below), leaving 31 caregiver-infant dyads. The independent sample was previously examined using different methods (87).…”