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Parental response to baby cry involves brain circuits for negative emotion Distancing-Embracing

Published online by Cambridge University Press:  29 November 2017

James E. Swain
Affiliation:
Department of Psychiatry and Psychology, Stony Brook University Medical Center, Stony Brook, NY 11794. james.swain@stonybrookmedicine.eduShao-Hsuan.ho@stonybrookmedicine.eduhttps://www.stonybrookmedicine.edu/profile?pid=2038&name=James%20Swain%20MDhttps://www.researchgate.net/profile/Shao-Hsuan_Ho Departments of Psychiatry and Psychology and Center for Human Growth and Development, University of Michigan, Ann Arbor, MI 48105. Child Study Center, Yale University School of Medicine, New Haven, CT 06520.
S. Shaun Ho
Affiliation:
Department of Psychiatry and Psychology, Stony Brook University Medical Center, Stony Brook, NY 11794. james.swain@stonybrookmedicine.eduShao-Hsuan.ho@stonybrookmedicine.eduhttps://www.stonybrookmedicine.edu/profile?pid=2038&name=James%20Swain%20MDhttps://www.researchgate.net/profile/Shao-Hsuan_Ho

Abstract

The “art form” of parent-infant bonding critically involves baby conveying negative emotions – literally compelling parents to respond and provide care. Current research on the brain basis of parenting is combining brain imaging with social, cognitive, and behavioral analyses to understand how parental brain circuits regulate thoughts and behavior in mental health, risk, and resilience. Understanding the parental brain may contribute to solving the long-standing paradox of self-sought hedonic exposure to negative emotions in art reception.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2017 

Baby cry conveys profoundly compelling negative emotions, akin to those paradoxically present in art aesthetics (Hume Reference Hume1757/1997) that secure attention, intense emotional involvement, and high memorability, yet invite care toward the development of the parent-infant bond (Swain et al. Reference Swain, Mayes and Leckman2004). Parental brain mechanisms to regulate caring thoughts and behaviors are increasingly well understood (Swain & Ho Reference Swain and Ho2017a; Swain et al. Reference Swain, Dayton, Kim, Tolman and Volling2014; Swain & Lorberbaum Reference Swain and Lorberbaum2008). Parents must hold the negative emotion perceptions at a cognitive-appraisal distance to also be compatible with the hedonic processing required for child care, that is, compassionate parenting (Swain & Ho Reference Swain, Ho, Seppala, Simon-Thomas, Brown, Worline, Cameron, Doty and Doty2017b), which may be similar to those discussed in the Distancing-Embracing model of art reception.

By way of introduction, the “art form” of parent-infant attachment is also a landmark conceptualization of human developmental psychology (Bowlby Reference Bowlby1969; Reference Bowlby1973). From an evolutionary perspective, attachment represents the innate neurobiological systems promoting proximity seeking between an infant and a conspecific attachment figure – usually the parent. This proximity and contingent care, driven by the thoughts and behaviors of parents, increase the likelihood of infants surviving to reproductive age. The baby's survival depends on conveying negative emotions – often with a cry – associated with needs for safety, food, warmth, or other care. Over the last 15 years, brain imaging studies have used baby-cry stimuli to probe for mechanisms of adaptive parenting among mothers (Kim et al. Reference Kim, Strathearn and Swain2016) and fathers (Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014) in mental health, in illness (Moses-Kolko et al. Reference Moses-Kolko, Horner, Phillips, Hipwell and Swain2014), and in risky situations such as poverty (Kim et al. Reference Kim, Rigo, Mayes, Feldman, Leckman and Swain2014). We discuss some of this parental brain research, which includes aversive infant stimuli such as baby cry, which may inform the Distancing-Embracing model of art reception.

Parent-infant attachment is another “art form” for which the aesthetic is very much in the “eye” of the beholder – in which parental brain activity depends on observed mental state talk (Hipwell et al. Reference Hipwell, Guo, Phillips, Swain and Moses-Kolko2015). How parents perceive their child is also related to their early-life experience and peripartum circumstances that affect parental brain physiology (Swain et al. Reference Swain, Kim, Spicer, Ho, Dayton, Elmadih and Abel2014). For example, high quality of perceived maternal care in childhood was associated with increased gray matter volumes in regions involved in regulation of emotions and social and sensory information processing, including the superior frontal gyrus, the orbitofrontal cortex, the superior and middle temporal gyri, and the fusiform gyrus (Kim et al. Reference Kim, Leckman, Mayes, Newman, Feldman and Swain2010b). Furthermore, higher levels of neural responses to infants' cry sounds were found in these same regions. The only region that was more active for mothers of low-quality maternal care in childhood was the stress-sensitive hippocampus. Perhaps early-life parental care also disrupts the appreciation of art with negative emotional content. In another study, early postpartum circumstances also altered brain structure (Kim et al. Reference Kim, Leckman, Mayes, Feldman, Wang and Swain2010a). Several brain regions involved in maternal motivation and reward processing, including the striatum, amygdala, hypothalamus, and substantia nigra, exhibited structural growth from the first few weeks to the fourth month postpartum. Structural growth was also observed in areas involved in processing sensory information and empathy, including the superior temporal gyrus, thalamus, insula, and pre- and postcentral gyri. Finally, regions associated with regulating emotions, such as the inferior and medial frontal gyri and the anterior cingulate cortex, also showed structural increases. This suggests that neural plasticity occurs in a wide range of brain regions, each serving important aspects of child caregiving in human mothers during the first few months postpartum. Furthermore, the greater the observed structural growth in the midbrain region (involved in reward and motivation), the stronger were the positive emotions a mother reported having about her baby in the third and fourth months postpartum. Researchers have yet to examine the strength of negative emotion perception directly, but this may already be a form of adaptive emotion distancing and embracing.

The evident plasticity may help explain psychopathology and treatment affect parenting. In a self-focused baby-cry task designed to provoke brain responses in participants with a history of adverse early-life experiences sometimes described as a malevolent background “shark music,” amygdala reactivity was increased (Swain et al. Reference Swain, Ho, Rosenblum, Morelen, Dayton and Muzik2017). Furthermore, time-dependent reduction in parenting stress was related to concomitant increased child- versus self-focused baby-cry responses in amygdala-temporal pole functional connectivity, which may facilitate maternal ability to take her child's perspective while maintaining appropriate distance.

One recent study begins to suggest how parenting brain mechanisms rooted in responses to baby cry during the development of the parent-infant bonding art form may be practically connected to later child outcome (Kim et al. Reference Kim, Rigo, Leckman, Mayes, Cole, Feldman and Swain2015). In this study, relationships between parental thoughts/actions and brain responses to own versus other baby-cry stimuli among mothers and fathers in the neonatal period were studied in relation to the child's social and emotional development by toddler age. Results differed for mothers and fathers, suggesting sex differences in the brain basis of early parental brain baby-cry responses linked with child socioemotional competency outcomes. This suggests sex differences in the brain areas that may also ultimately fit into the Distancing-Embracing model.

Some of these complex neuroimaging findings may ultimately need to be interpreted as changes in distributed network function. For example, compared with maintaining one's emotional responses, engaging in reappraisal – a form of distancing-embracing neuroimaging task – produced robust and distributed alterations in functional connections involving visual, dorsal attention, frontoparietal, and default networks (Sripada et al. Reference Sripada, Swain, Ho and Swain2014). Indeed, a widespread set of brain responses were also reported in a recent study of mothers responding to child visual feedback after a caring decision (Ho et al. Reference Ho, Konrath, Brown and Swain2014). Responses that correlated with dimensions of empathy included the amygdala, ventrolateral prefrontal cortex, and supplementary motor area that may also fit with broader work on altruistic behaviors (Brown & Brown Reference Brown and Brown2015; Swain et al. Reference Swain, Konrath, Brown, Finegood, Akce, Dayton and Ho2012), which may also involve appropriate Distancing-Embracing of negative emotions.

ACKNOWLEDGMENT

The authors are supported by the Department of Psychiatry at Stony Brook University, National Alliance for Research on Schizophrenia and Depression.

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