Postpartum depressive symptoms moderate the link between mothers’ neural response to positive faces in reward and social regions and observed caregiving

Social Cognitive and Affective Neuroscience, 2017, 1605–1613 doi: 10.1093/scan/nsx087 Advance Access Publication Date: 30 June 2017 Original article Postpartum depressive symptoms moderate the link between mothers’ neural response to positive faces in reward and social regions and observed caregiving Judith K. Morgan, Chaohui Guo, Eydie L. Moses-Kolko, Mary L. Phillips, Stephanie D. Stepp, and Alison E. Hipwell Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA 15213, USA Correspondence should be addressed to Judith K. Morgan, University of Pittsburgh, 3811 O’Hara Street, Pittsburgh, PA 15213, USA. E-mail: Abstract Postpartum depression may disrupt socio-affective neural circuitry and compromise provision of positive parenting. Although work has evaluated how parental response to negative stimuli is related to caregiving, research is needed to examine how depressive symptoms during the postpartum period may be related to neural response to positive stimuli, especially positive faces, given depression’s association with biased processing of positive faces. The current study examined the association between neural response to adult happy faces and observations of maternal caregiving and the moderating role of postpartum depression, in a sample of 18- to 22-year old mothers (n ¼ 70) assessed at 17 weeks (s.d. ¼ 4.7 weeks) postpartum. Positive caregiving was associated with greater precuneus and occipital response to positive faces among mothers with lower depressive symptoms, but not for those with higher symptoms. For mothers with higher depressive symptoms, greater ventral and dorsal striatal response to positive faces was associated with more positive caregiving, whereas the opposite pattern emerged for mothers with lower symptoms. There was no association between negative caregiving and neural response to positive faces or negative faces. Processing of positive stimuli may be an important prognostic target in mothers with depressive symptoms, given its link with healthy caregiving behaviors. Key words: caregiving; ventral striatum; precuneus Introduction Positive caregiving, characterized by warm, sensitive and consistent responding to the needs of one’s infant, is important for healthy child development (Sroufe, 2005). In particular, prior work has demonstrated that warm and sensitive parental responding during the early years of life predicts greater positive affect, affect regulation, empathy and physiological selfregulation in offspring across development (Feldman, 2007, Leclere et al., 2014). In contrast, early negative caregiving, characterized by hostile, harsh and intrusive responding, has been linked to greater affective and physiological dysregulation in offspring (Egeland et al., 1993; Feldman, 2015). These elements of parenting appear to be especially important during the early years, a sensitive developmental period when infants depend on caregivers for all of their primary needs and when their physiological systems are developing quite rapidly (Feldman, 2015). Recent work has demonstrated that a network of neural regions, "the caregiving brain" is involved in positive caregiving. The caregiving brain is concentrated in a cortico-striatalthalamic loop that includes the prefrontal cortex, cingulate, striatum and thalamus, as well as the precuneus and amygdala Received: 30 October 2016; Revised: 13 June 2017; Accepted: 26 June 2017 C The Author (2017). Published by Oxford University Press. V This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact 1605 1606 | Social Cognitive and Affective Neuroscience, 2017, Vol. 12, No. 10 (Swain, 2011; Swain et al., 2014). Function in these regions is thought to aid in increasing emotional arousal to, and salience of, infant cues (i.e. striatum, amydgala and insula), in promoting regulation of one’s own affect in order to attend to these cues (i.e. prefrontal cortex), and in fostering empathy and mentalizing skills to understand how to respond sensitively to these cues (i.e. thalamus, precuneus, posterior cingulate) (Barrett and Fleming, 2011). Multiple psychosocial and contextual factors may influence function within the caregiving brain (Barrett and Fleming, 2011). In particular, postpartum depression appears to interfere with adaptive function of these neural regions (Moses-Kolko et al., 2014). Specifically, a growing body of work has demonstrated that postpartum mothers with high depressive symptoms show blunted responding to infant distress in regions implicated in emotional salience and threat responding (e.g. amygdala, anterior cingulate), in reward and social bonding (e.g. striatum), in goal-directed behavior and self-regulation (e.g. cingulate, orbitofrontal cortex), and in social cognition (e.g. thalamus), suggesting they may have fewer neurobiological resources to respond sensitively to their distressed infant (Laurent and Ablow, 2012, 2013, Moses-Kolko et al., 2014). This depression effect on brain function, particularly brain function in regions that have been associated with caregiving, is not surprising, given evidence that depression is often associated with compromised caregiving (Lovejoy et al., 2000; Field, 2010). For example, postpartum depressive symptoms have been associated with more irritable and hostile mother-infant interactions (Field, 2010). Importantly, this depression-related effect on caregiving has a considerable public health impact. Approximately, 10–15% of new mothers experience postpartum depressive symptoms (Paulson et al., 2006) and the likelihood of these symptoms increases for mothers living in high-stress environments, for mothers with low socioeconomic status, and for mothers who are younger age or minority status (Segre et al., 2007), leaving the children of these mothers at even greater risk for negative child outcomes. Despite the growing body of work evaluating parental neural response to negative stimuli (see Barrett and Fleming, 2011), relatively little work has evaluated how neural response to positive stimuli may predict caregiving patterns in postpartum mothers. Research has shown that depressed individuals are less likely to recognize positive affect in others (Joormann and Gotlib, 2006; Surguladze et al., 2004), and some work has demonstrated that depressed mothers show difficulty in identifying happy affect in their infant’s facial expressions (Arteche et al., 2011). This is problematic because warm, sensitive caregiving requires accurately identifying the feelings of one’s infant in order to respond appropriately to those cues. Indeed, depressed mothers show lower sensitivity and less contingent responding to the positive cues of their infants (Field et al., 2010 (...truncated)