James E. Swain

Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood

Significance Childhood poverty has been linked to emotion dysregulation, which is further associated with negative physical and psychological health in adulthood. The current study provides evidence of prospective associations between childhood poverty and adult neural activity during effortful attempts to regulate negative emotion. Adults with lower family income at age 9 exhibited reduced ventrolateral and dorsolateral prefrontal cortex activity and failure to suppress amygdala activation at age 24. Chronic stressor exposure across childhood mediated the relations between family income at age 9 and prefrontal cortex activity. The concurrent adult income, on the other hand, was not associated with neural activity. The information on the developmental timing of poverty effects and neural mechanisms may inform early interventions aimed at reducing health disparities. Childhood poverty has pervasive negative physical and psychological health sequelae in adulthood. Exposure to chronic stressors may be one underlying mechanism for childhood poverty−health relations by influencing emotion regulatory systems. Animal work and human cross-sectional studies both suggest that chronic stressor exposure is associated with amygdala and prefrontal cortex regions important for emotion regulation. In this longitudinal functional magnetic resonance imaging study of 49 participants, we examined associations between childhood poverty at age 9 and adult neural circuitry activation during emotion regulation at age 24. To test developmental timing, concurrent, adult income was included as a covariate. Adults with lower family income at age 9 exhibited reduced ventrolateral and dorsolateral prefrontal cortex activity and failure to suppress amygdala activation during effortful regulation of negative emotion at age 24. In contrast to childhood income, concurrent adult income was not associated with neural activity during emotion regulation. Furthermore, chronic stressor exposure across childhood (at age 9, 13, and 17) mediated the relations between family income at age 9 and ventrolateral and dorsolateral prefrontal cortex activity at age 24. The findings demonstrate the significance of childhood chronic stress exposures in predicting neural outcomes during emotion regulation in adults who grew up in poverty.

Breastfeeding, brain activation to own infant cry, and maternal sensitivity

BACKGROUND Research points to the importance of breastfeeding for promoting close mother-infant contact and social-emotional development. Recent functional magnetic resonance imaging (fMRI) studies have identified brain regions related to maternal behaviors. However, little research has addressed the neurobiological mechanisms underlying the relationship between breastfeeding and maternal behavior in human mothers. We investigated the associations between breastfeeding, maternal brain response to own infant stimuli, and maternal sensitivity in the early postpartum. METHODS Seventeen biological mothers of healthy infants participated in two matched groups according to feeding method - exclusive breastfeeding and exclusive formula-feeding at 2-4 weeks postpartum. fMRI scanning was conducted in the first postpartum month to examine maternal brain activation in response to her own babys cry versus control baby-cry. Dyadic interactions between mothers and infants at 3-4 months postpartum were videotaped in the home and blindly coded for maternal sensitivity. RESULTS In the first postpartum month, breastfeeding mothers showed greater activations in the superior frontal gyrus, insula, precuneus, striatum, and amygdala while listening to their own baby-cry as compared to formula-feeding mothers. For both breastfeeding and formula-feeding mothers, greater activations in the right superior frontal gyrus and amygdala were associated with higher maternal sensitivity at 3-4 months postpartum. CONCLUSIONS Results suggest links between breastfeeding and greater response to infant cues in brain regions implicated in maternal-infant bonding and empathy during the early postpartum. Such brain activations may facilitate greater maternal sensitivity as infants enter their social world.

Primary parental preoccupation: circuits, genes, and the crucial role of the environment

Summary.Parental caregiving includes a set of highly conserved behaviors and mental states that may reflect both an individual’s genetic endowment and the early experience of being cared for as a child. This review first examines the mental and behavioral elements of early parental caregiving in humans. Second, we consider what is known about the neurobiological substrates of maternal behaviors in mammalian species including some limited human data. Third, we briefly review the evidence that specific genes encode proteins that are crucial for the development of the neural substrates that underlie specific features of maternal behavior. Fourth, we review the emerging literature on the “programming” role of the intrauterine environment and postnatal caregiving environment in shaping subsequent maternal behavior. We conclude that there are critical developmental windows during which the genetically determined microcircuitry of key limbic-hypothalamic-midbrain structures are susceptible to early environmental influences and that these influences powerfully shape an individual’s responsivity to psychosocial stressors and their resiliency or vulnerability to various forms of human psychopathology later in life.

Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers.

Brain networks that govern parental response to infant signals have been studied with imaging techniques over the last 15 years. The complex interaction of thoughts and behaviors required for sensitive parenting enables the formation of each individuals first social bonds and critically shapes development. This review concentrates on magnetic resonance imaging experiments which directly examine the brain systems involved in parental responses to infant cues. First, we introduce themes in the literature on parental brain circuits studied to date. Next, we present a thorough chronological review of state-of-the-art fMRI studies that probe the parental brain with a range of baby audio and visual stimuli. We also highlight the putative role of oxytocin and effects of psychopathology, as well as the most recent work on the paternal brain. Taken together, a new model emerges in which we propose that cortico-limbic networks interact to support parental brain responses to infants. These include circuitry for arousal/salience/motivation/reward, reflexive/instrumental caring, emotion response/regulation and integrative/complex cognitive processing. Maternal sensitivity and the quality of caregiving behavior are likely determined by the responsiveness of these circuits during early parent-infant experiences. The function of these circuits is modifiable by current and early-life experiences, hormonal and other factors. Severe deviation from the range of normal function in these systems is particularly associated with (maternal) mental illnesses - commonly, depression and anxiety, but also schizophrenia and bipolar disorder. Finally, we discuss the limits and extent to which brain imaging may broaden our understanding of the parental brain given our current model. Developments in the understanding of the parental brain may have profound implications for long-term outcomes in families across risk, resilience and possible interventions. This article is part of a Special Issue entitled Oxytocin and Social Behav.

Perceived quality of maternal care in childhood and structure and function of mothers' brain

Animal studies indicate that early maternal care has long-term effects on brain areas related to social attachment and parenting, whereas neglectful mothering is linked with heightened stress reactivity in the hippocampus across the lifespan. The present study explores the possibility, using magnetic resonance imaging, that perceived quality of maternal care in childhood is associated with brain structure and functional responses to salient infant stimuli among human mothers in the first postpartum month. Mothers who reported higher maternal care in childhood showed larger grey matter volumes in the superior and middle frontal gyri, orbital gyrus, superior temporal gyrus and fusiform gyrus. In response to infant cries, these mothers exhibited higher activations in the middle frontal gyrus, superior temporal gyrus and fusiform gyrus, whereas mothers reporting lower maternal care showed increased hippocampal activations. These findings suggest that maternal care in childhood may be associated with anatomy and functions in brain regions implicated in appropriate responsivity to infant stimuli in human mothers.

In Search of Neural Endophenotypes of Postpartum Psychopathology and Disrupted Maternal Caregiving

This is a selective review that provides the context for the study of perinatal affective disorder mechanisms and outlines directions for future research. We integrate existing literature along neural networks of interest for affective disorders and maternal caregiving: (i) the salience/fear network; (ii) the executive network; (iii) the reward/social attachment network; and (iv) the default mode network. Extant salience/fear network research reveals disparate responses and corticolimbic coupling to various stimuli based upon a predominantly depressive versus anxious (post‐traumatic stress disorder) clinical phenotype. Executive network and default mode connectivity abnormalities have been described in postpartum depression (PPD), although studies are very limited in these domains. Reward/social attachment studies confirm a robust ventral striatal response to infant stimuli, including cry and happy infant faces, which is diminished in depressed, insecurely attached and substance‐using mothers. The adverse parenting experiences received and the attachment insecurity of current mothers are factors that are associated with a diminution in infant stimulus‐related neural activity similar to that in PPD, and raise the need for additional studies that integrate mood and attachment concepts in larger study samples. Several studies examining functional connectivity in resting state and emotional activation functional magnetic resonance imaging paradigms have revealed attenuated corticolimbic connectivity, which remains an important outcome that requires dissection with increasing precision to better define neural treatment targets. Methodological progress is expected in the coming years in terms of refining clinical phenotypes of interest and experimental paradigms, as well as enlarging samples to facilitate the examination of multiple constructs. Functional imaging promises to determine neural mechanisms underlying maternal psychopathology and impaired caregiving, such that earlier and more precise detection of abnormalities will be possible. Ultimately, the discovery of such mechanisms will promote the refinement of treatment approaches toward maternal affective disturbance, parenting behaviours and the augmentation of parenting resiliency.

Parenting and Beyond: Common Neurocircuits Underlying Parental and Altruistic Caregiving

SYNOPSIS Interpersonal relationships constitute the foundation on which human society is based. The infant–caregiver bond is the earliest and most influential of these relationships. Driven by evolutionary pressure for survival, parents feel compelled to provide care to their biological offspring. However, compassion for non-kin is also ubiquitous in human societies, motivating individuals to suppress their own self-interests to promote the well-being of non-kin members of the society. We argue that the process of early kinship-selective parental care provides the foundation for non-exclusive altruism via the activation of a general Caregiving System that regulates compassion in any of its forms. We propose a tripartite structure of this system that includes (1) the perception of need in another, (2) a caring motivational or feeling state, and (3) the delivery of a helping response to the individual in need. Findings from human and animal research point to specific neurobiological mechanisms including activation of the insula and the secretion of oxytocin that support the adaptive functioning of this Caregiving System.

Neuroendocrinology of Parental Response to Baby‐Cry

This overview attempts to synthesise current understandings of the neuroendocrine basis of parenting. The parent–infant bond is central to the human condition, contributes to risks for mood and anxiety disorders, and provides the potential for resiliency and protection against the development of psychopathology. Animal models of parenting provide compelling evidence that biological mechanisms may be studied in humans. This has led to brain imaging and endocrine system studies of human parents using baby stimuli and concerted psychological and behavioural measures. Certain brain circuits and related hormonal systems, including subcortical regions for motivation (striatum, amygdala, hypothalamus and hippocampus) and cortical regions for social cognition (anterior cingulate, insula, medial frontal and orbitofrontal cortices), appear to be involved. These brain circuits work with a range of endocrine systems to manage stress and motivate appropriate parental caring behaviour with a flexibility appropriate to the environment. Work in this field promises to link evolving models of parental brain performance with resilience, risk and treatment toward mother–infant mental health.

Parental attachment systems: neural circuits, genes, and experiential contributions to parental engagement

Abstract Parental caregiving includes a set of highly conserved set of behaviors and mental states that may reflect both an individuals genetic endowment and the early experience of being cared for as a child. We consider the mental and behavioral elements of early parental caregiving in humans and what is known of the neurobiological substrates of maternal behaviors in mammalian species including some limited human data. Also reviewed briefly is the evidence that specific genes encode proteins that are crucial for the development of the neural substrates that underlie specific features of maternal behavior. Finally, we review the literature on the “programming” role of epigenetic factors in shaping subsequent maternal behavior. Drawing also from recent neuroimaging data, we conclude that there are critical developmental windows during which the genetically determined microcircuitry of key limbic-hypothalamic-midbrain structures are susceptible to early environmental influences and that these influences powerfully shape an individuals responsivity to psychosocial stressors and their resiliency or vulnerability to various forms of human psychopathology later in life.

The normalcy of neurosis: evolutionary origins of obsessive-compulsive disorder and related behaviors.

One of the most curious questions plaguing subscribers of evolutionary theory is how natural selections fine-tuned editing function could allow disease to persist. For evolutionary psychiatrists, the existence of psychopathology is thus perplexing. To illustrate a potential answer to one instance of this broad question, we examine the correlates of obsessive-compulsive disorder (OCD) within our normal repertoire of thought and action. The evidence presents a picture of OCD as a dysregulation of normal behaviors and mental states throughout the course of human development. We speculate that such correspondence may be more than a coincidence and that OCD is a consequence of a dysregulation of the neural circuits that are crucially involved in threat detection and harm avoidance. These neural systems are also likely to underlie aspects of religious experience and ritual as well as the wonders of romantic and early parental love.