Intergenerational neuroimaging study: mother-infant functional connectivity similarity and the role of infant and maternal factors.

Mother and infant neural and behavioral synchrony is important for infant development during the first years of life. Recent studies also suggest that neural risk markers associated with parental psychopathology may be transmitted across generations before symptoms emerge in offspring. There is limited understanding of how early similarity in brain functioning between 2 generations emerges. In the current study, using functional magnetic resonance imaging, we examined the functional connectivity (FC) similarity between mothers and newborns during the first 3 months after the infant's birth. We found that FC similarity between mothers and infants increased as infant age increased. Furthermore, we examined whether maternal factors such as maternal socioeconomic status and prenatal maternal depressive symptoms may influence individual differences in FC similarity. For the whole-brain level, lower maternal education levels were associated with greater FC similarity. In previous literature, lower maternal education levels were associated with suboptimal cognitive and socioemotional development. Greater FC similarity may reflect that the infants develop their FC similarity prematurely, which may suboptimally influence their developmental outcomes in later ages.

How stress can influence brain adaptations to motherhood.

Research shows that a woman's brain and body undergo drastic changes to support her transition to parenthood during the perinatal period. The presence of this plasticity suggests that mothers' brains may be changed by their experiences. Exposure to severe stress may disrupt adaptive changes in the maternal brain and further impact the neural circuits of stress regulation and maternal motivation. Emerging literature of human mothers provides evidence that stressful experience, whether from the past or present environment, is associated with altered responses to infant cues in brain circuits that support maternal motivation, emotion regulation, and empathy. Interventions that reduce stress levels in mothers may reverse the negative impact of stress exposure on the maternal brain. Finally, outstanding questions regarding the timing, chronicity, types, and severity of stress exposure, as well as study design to identify the causal impact of stress, and the role of race/ethnicity are discussed.

Postpartum Stress and Neural Regulation of Emotion among First-Time Mothers.

Early parenting relies on emotion regulation capabilities, as mothers are responsible for regulating both their own emotional state and that of their infant during a time of new parenting-related neural plasticity and potentially increased stress. Previous research highlights the importance of frontal cortical regions in facilitating effective emotion regulation, but few studies have investigated the neural regulation of emotion among postpartum women. The current study employed a functional neuroimaging (fMRI) approach to explore the association between perceived stress, depressive symptoms, and the neural regulation of emotion in first-time mothers. Among 59 postpartum mothers, higher perceived stress during the postpartum period was associated with less self-reported use of cognitive reappraisal in everyday life, and greater use of emotion suppression. While viewing standardized aversive images during the Emotion Regulation Task (ERT), mothers were instructed to experience their natural emotional state (Maintain) or to decrease the intensity of their negative emotion by using cognitive reappraisal (Reappraise). Whole-brain analysis revealed a two-way interaction of perceived stress x condition in the right dorsolateral prefrontal cortex (DLPFC) at p < .05 cluster-wise corrected, controlling for postpartum months and scanner type. Higher levels of perceived stress were associated with heightened right DLPFC activity while engaging in cognitive reappraisal versus naturally responding to negative stimuli. Higher right DLPFC activity during Reappraise versus Maintain was further associated with elevated parenting stress. Findings suggest that stress and everyday reappraisal use is reflected in mothers' neural regulation of emotion and may have important implications for their adaptation to parenthood.

Childhood socioeconomic status is prospectively associated with surface morphometry in adulthood.

Childhood socioeconomic status (SES) has been associated with brain cortex surface area in children. However, the extent to which childhood SES is prospectively associated with brain morphometry in adulthood is unclear. We tested whether childhood SES (income-to-needs ratio averaged across ages 9, 13, and 17) is prospectively associated with cortical surface morphometry in adulthood. Average childhood income-to-needs ratio had a positive, prospective association with cortical thickness in adulthood in the precentral gyrus, postcentral gyrus, and caudal middle frontal gyrus (p < .05, FWE corrected). Childhood income-to-needs ratio also had a positive, prospective association with cortical surface area in adulthood in multiple regions, including the rostral and caudal middle frontal gyri and superior frontal gyrus (p < .05, FWE corrected). Concurrent income-to-needs ratio (measured at age 24) was not associated with cortical thickness or surface area in adulthood. The results underscore the importance of addressing poverty in childhood for brain morphological development.

Maternal trait anxiety symptoms, frontolimbic resting-state functional connectivity, and cognitive development in infancy.

Exposure to maternal anxiety symptoms during infancy has been associated with difficulties in development and greater risk for developing anxiety later in life. Although previous studies have examined associations between prenatal maternal distress, infant brain development, and developmental outcomes, it is still largely unclear if there are associations between postnatal anxiety, infant brain development, and cognitive development in infancy. In this study, we used resting-state functional magnetic resonance imaging to examine the association between maternal anxiety symptoms and resting-state functional connectivity in the first year of life. We also examine the association between frontolimbic functional connectivity and infant cognitive development. The sample consisted of 21 infants (mean age = 24.15 months, SD = 4.17) that were scanned during their natural sleep using. We test the associations between maternal trait anxiety symptoms and amygdala-anterior cingulate cortex (ACC) functional connectivity, a neural circuit implicated in early life stress exposure. We also test the associations between amygdala-ACC connectivity and cognitive development. We found a significant negative association between maternal trait anxiety symptoms and left amygdala-right ACC functional connectivity (p < .05, false discovery rate corrected). We found a significant negative association between left amygdala-right ACC functional connectivity and infant cognitive development (p < .05). These findings have potential implications for understanding the role of postpartum maternal anxiety symptoms in functional brain and cognitive development in infancy.

Associations between stress exposure and new mothers' brain responses to infant cry sounds.

Exposure to severe stress has been linked to negative postpartum outcomes among new mothers including mood disorders and harsh parenting. Non-human animal studies show that stress exposure disrupts the normative adaptation of the maternal brain, thus identifying a neurobiological mechanism by which stress can lead to negative maternal outcomes. However, little is known about the impact of stress exposure on the maternal brain response to infant cues in human mothers. We examined the association of stress exposure with brain response to infant cries and maternal behaviors, in a socioeconomically diverse (low- and middle-income) sample of first-time mothers (N=53). Exposure to stress across socioeconomic, environmental, and psychosocial domains was associated with reduced brain response to infant cry sounds in several regions, including the right insula/inferior frontal gyrus and superior temporal gyrus. Reduced activation in these regions was further associated with lower maternal sensitivity observed during a mother-infant interaction. The findings demonstrate that higher levels of stress exposure may be associated with reduced brain response to an infant's cry in regions that are important for emotional and social information processing, and that reduced brain responses may further be associated with increased difficulties in developing positive mother-infant relationships.

Prospective associations, longitudinal patterns of childhood socioeconomic status, and white matter organization in adulthood.

The association between childhood socioeconomic status (SES) and brain development is an emerging area of research. The primary focus to date has been on SES and variations in gray matter structure with much less known about the relation between childhood SES and white matter structure. Using a longitudinal study of SES, with measures of income-to-needs ratio (INR) at age 9, 13, 17, and 24, we examined the prospective relationship between childhood SES (age 9 INR) and white matter organization in adulthood using diffusion tensor imaging. We also examined how changes in INR from childhood through young adulthood are associated with white matter organization in adult using a latent growth mixture model. Using tract-based spatial statistics (TBSS) we found that there is a significant prospective positive association between childhood INR and white matter organization in the bilateral uncinate fasciculus, bilateral cingulum bundle, bilateral superior longitudinal fasciculus, and corpus callosum (p < .05, FWE corrected). The probability that an individual was in the high-increasing INR profile across development compared with the low-increasing INR profile was positively associated with white matter organization in the bilateral uncinate fasciculus, left cingulum, and bilateral superior longitudinal fasciculus. The results of the current study have potential implications for interventions given that early childhood poverty may have long-lasting associations with white matter structure. Furthermore, trajectories of socioeconomic status during childhood are important-with individuals that belong to the latent profile that had high increases in INR having greater regional white matter organization in adulthood.

Socioeconomic disadvantage, brain morphometry, and attentional bias to threat in middle childhood.

Socioeconomic disadvantage is associated with higher rates of psychopathology as well as hippocampus, amygdala and prefrontal cortex structure. However, little is known about how variations in brain morphometry are associated with socio-emotional risks for mood disorders in children growing up in families experiencing low income. In the current study, using structural magnetic resonance imaging, we examined the relationship between socioeconomic disadvantage and gray matter volume in the hippocampus, amygdala, and ventrolateral prefrontal cortex in a sample of children (n = 34) in middle childhood. Using an affective dot probe paradigm, we examined the association between gray matter volume in these regions and attentional bias to threat, a risk marker for mood disorders including anxiety disorders. We found that lower income-to-needs ratio was associated with lower bilateral hippocampal and right amygdala volume, but not prefrontal cortex volumes. Moreover, lower attentional bias to threat was associated with greater left hippocampal volume. We provide evidence of a relationship between income-related variations in brain structure and attentional bias to threat, a risk for mood disorders. Therefore, these findings support an environment-morphometry-behavior relationship that contributes to the understanding of income-related mental health disparities in childhood.

Intensity, not emotion: The role of poverty in emotion labeling ability in middle childhood.

Poverty exposure has been linked to difficulties in emotion expression recognition, which further increases risks for negative emotional outcomes among children. The current study aimed to investigate whether the difficulties in emotion expression recognition among children experiencing poverty may be emotion specific or expression intensity specific. Thus, the current study investigated the relationship between poverty exposure and emotion labeling ability in an ethnically and economically diverse sample of children (N = 46) in middle childhood. A novel experimental design measured emotion labeling ability at different valences of emotion (fearful, angry, and happy) and at varying intensities (0-100%) of emotion presentation. Using a hierarchical logistic regression, we found a significant interaction between the percentage of time since birth a child has lived in poverty and the intensity of the emotional stimulus in affecting correct emotion identification. Children who lived longer in poverty gained less accuracy for equivalent increases in intensity compared with children who had not lived in poverty. On average, children who chronically lived in poverty required emotional intensity set at 60% in order to reach levels of accuracy observed at 30% intensity among children who were never exposed to poverty. We found no significant emotion-specific effect. These findings demonstrate that children who experience chronic poverty require more intense expressions to recognize emotions across valences. This further elaborates the existing understanding of a relationship between poverty exposure and emotion recognition, informing future studies examining expression recognition as a mechanism involved in developing psychopathology.

The maternal brain and its plasticity in humans.

This article is part of a Special Issue "Parental Care". Early mother-infant relationships play important roles in infants' optimal development. New mothers undergo neurobiological changes that support developing mother-infant relationships regardless of great individual differences in those relationships. In this article, we review the neural plasticity in human mothers' brains based on functional magnetic resonance imaging (fMRI) studies. First, we review the neural circuits that are involved in establishing and maintaining mother-infant relationships. Second, we discuss early postpartum factors (e.g., birth and feeding methods, hormones, and parental sensitivity) that are associated with individual differences in maternal brain neuroplasticity. Third, we discuss abnormal changes in the maternal brain related to psychopathology (i.e., postpartum depression, posttraumatic stress disorder, substance abuse) and potential brain remodeling associated with interventions. Last, we highlight potentially important future research directions to better understand normative changes in the maternal brain and risks for abnormal changes that may disrupt early mother-infant relationships.

Subliminal trauma reminders impact neural processing of cognitive control in adults with developmental earthquake trauma: a preliminary report.

Little is known about the effects of developmental trauma on the neural basis of cognitive control among adults who do not have posttraumatic stress disorder. To examine this question, we used functional magnetic resonance imaging to compare the effect of subliminal priming with earthquake-related images on attentional control during a Stroop task in survivors of the 2008 Wenchuan earthquake in China (survivor group, survivors were adolescents at the time of the earthquake) and in matched controls (control group). We found that the survivor group showed greater activation in the left ventral anterior cingulate cortex (vACC) and the bilateral parahippocampal gyrus during the congruent versus incongruent condition, as compared to the control group. Depressive symptoms were positively correlated with left vACC activation during the congruent condition. Moreover, psychophysiological interaction results showed that the survivor group had stronger functional connectivity between the left parahippocampal gyrus and the left vACC than the control group under the congruent-incongruent condition. These results suggested that trauma-related information was linked to abnormal activity in brain networks associated with cognitive control (e.g., vACC-parahippocampal gyrus). This may be a potential biomarker for depression following developmental trauma, and it may also provide a mechanism linking trauma reminders with depression.

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

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.

Human Maternal Brain Plasticity: Adaptation to Parenting.

New mothers undergo dynamic neural changes that support positive adaptation to parenting and the development of mother-infant relationships. In this article, I review important psychological adaptations that mothers experience during pregnancy and the early postpartum period. I then review evidence of structural and functional plasticity in human mothers' brains, and explore how such plasticity supports mothers' psychological adaptation to parenting and sensitive maternal behaviors. Last, I discuss pregnancy and the early postpartum period as a window of vulnerabilities and opportunities when the human maternal brain is influenced by stress and psychopathology, but also receptive to interventions.

Childhood social inequalities influences neural processes in young adult caregiving.

Childhood poverty is associated with harsh parenting with a risk of transmission to the next generation. This prospective study examined the relations between childhood poverty and non-parent adults' neural responses to infant cry sounds. While no main effects of poverty were revealed in contrasts of infant cry versus acoustically matched white noise, a gender by childhood poverty interaction emerged. In females, childhood poverty was associated with increased neural activations in the posterior insula, striatum, calcarine sulcus, hippocampus, and fusiform gyrus, while, in males, childhood poverty was associated with reduced levels of neural responses to infant cry in the same regions. Irrespective of gender, neural activation in these regions was associated with higher levels of annoyance with the cry sound and reduced desire to approach the crying infant. The findings suggest gender differences in neural and emotional responses to infant cry sounds among young adults growing up in poverty.

Volitional regulation of emotions produces distributed alterations in connectivity between visual, attention control, and default networks.

The ability to volitionally regulate emotions is critical to health and well-being. While patterns of neural activation during emotion regulation have been well characterized, patterns of connectivity between regions remain less explored. It is increasingly recognized that the human brain is organized into large-scale intrinsic connectivity networks (ICNs) whose interrelationships are altered in characteristic ways during psychological tasks. In this fMRI study of 54 healthy individuals, we investigated alterations in connectivity within and between ICNs produced by the emotion regulation strategy of reappraisal. In order to gain a comprehensive picture of connectivity changes, we utilized connectomic psychophysiological interactions (PPI), a whole-brain generalization of standard single-seed PPI methods. In particular, we quantified PPI connectivity pair-wise across 837 ROIs placed throughout the cortex. We found that compared to maintaining one's emotional responses, engaging in reappraisal produced robust and distributed alterations in functional connections involving visual, dorsal attention, frontoparietal, and default networks. Visual network in particular increased connectivity with multiple ICNs including dorsal attention and default networks. We interpret these findings in terms of the role of these networks in mediating critical constituent processes in emotion regulation, including visual processing, stimulus salience, attention control, and interpretation and contextualization of stimuli. Our results add a new network perspective to our understanding of the neural underpinnings of emotion regulation, and highlight that connectomic methods can play a valuable role in comprehensively investigating modulation of connectivity across task conditions.

Longitudinal Neuroanatomical Increases from Early to One-Year Postpartum.

Preclinical studies have provided causal evidence that the postpartum period involves regional neuroanatomical changes in 'maternal' brain regions to support the transition to offspring caregiving. Few studies, in humans, have examined neuroanatomical changes from early to one-year postpartum with longitudinal neuroimaging data and their association with postpartum mood changes. In this study, we examined longitudinal changes in surface morphometry (cortical thickness and surface area) in regions previously implicated in the transition to parenthood. We also examined longitudinal volumetric neuroanatomical changes in three subcortical regions of the maternal brain: the hippocampus, amygdala, and ventral diencephalon. Twenty-four participants underwent longitudinal structural magnetic resonance imaging at 2-4 weeks and 1 year postpartum. Cortical thickness increased from early to one-year postpartum in the left (p = .003, Bonferroni corrected) and right (p = .02, Bonferroni corrected) superior frontal gyrus. No significant increases (or decreases) were observed in these regions for surface area. Volumetric increases, across the postpartum period, were found in the left amygdala (p = .001, Bonferroni corrected) and right ventral diencephalon (p = .01, Bonferroni corrected). An exploratory analysis of depressive symptoms found reductions in depressive symptoms from early postpartum to one-year postpartum were associated with greater cortical thickness in the superior frontal gyrus for both the left (p = .02) and right (p = .02) hemispheres. The findings expand our evidence of the neuroanatomical changes that occur across the postpartum period in humans and motivate future studies to examine how mood changes across this period are associated with cortical thickness of the superior frontal gyrus.

Childhood poverty and blood pressure reactivity to and recovery from an acute stressor in late adolescence: the mediating role of family conflict.

OBJECTIVE: Childhood deprivation is inimical to health throughout the life course. Early experiences of stress could play a role in health inequalities. An important aspect of childhood poverty that has not received much attention is cardiovascular reactivity to and recovery from acute stressors. METHODS: Piecewise, multilevel growth curve regression was used to examine blood pressure reactivity to and recovery from a mental arithmetic task among late adolescents (mean [standard deviation] = 17.3 [1.0] years, n = 185) as a function of early childhood poverty (9 years). We also tested whether exposure to family conflict at age 13 years mediated expected linkages between childhood poverty and adolescent blood pressure reactivity and recovery to an acute stressor. RESULTS: Blood pressure reactivity was unaffected by household income during childhood, but late adolescents with lower household income during childhood showed slower systolic (b = -0.29, p = .004) and diastolic (b = -0.19, p = .002) recovery. These results include age and sex as statistical covariates. The significant poverty impact on systolic but not on diastolic blood pressure recovery was mediated by exposure to family conflict (95% confidence interval = - 0.1400 to - 0.0012). CONCLUSIONS: We show that late adolescents who grew up in poverty have delayed blood pressure recovery from an acute stressor. Furthermore, childhood exposure to family conflict, a well-documented component of early childhood deprivation, accounted for some of the adverse effects of childhood poverty on stressor recovery among these adolescents. We discuss the importance of considering physiological stress accompanying early experiences of deprivation in thinking about health inequalities.

Impaired fixation to eyes during facial emotion labelling in children with bipolar disorder or severe mood dysregulation.

BACKGROUND: Children with bipolar disorder (BD) or severe mood dysregulation (SMD) show behavioural and neural deficits during facial emotion processing. In those with other psychiatric disorders, such deficits have been associated with reduced attention to eye regions while looking at faces. METHODS: We examined gaze fixation patterns during a facial emotion labelling task among children with pediatric BD and SMD and among healthy controls. Participants viewed facial expressions with varying emotions (anger, fear, sadness, happiness, neutral) and emotional levels (60%, 80%, 100%) and labelled emotional expressions. RESULTS: Our study included 22 children with BD, 28 with SMD and 22 controls. Across all facial emotions, children with BD and SMD made more labelling errors than controls. Compared with controls, children with BD spent less time looking at eyes and made fewer eye fixations across emotional expressions. Gaze patterns in children with SMD tended to fall between those of children with BD and controls, although they did not differ significantly from either of these groups on most measures. Decreased fixations to eyes correlated with lower labelling accuracy in children with BD, but not in those with SMD or in controls. LIMITATIONS: Most children with BD were medicated, which precluded our ability to evaluate medication effects on gaze patterns. CONCLUSION: Facial emotion labelling deficits in children with BD are associated with impaired attention to eyes. Future research should examine whether impaired attention to eyes is associated with neural dysfunction. Eye gaze deficits in children with BD during facial emotion labelling may also have treatment implications. Finally, children with SMD exhibited decreased attention to eyes to a lesser extent than those with BD, and these equivocal findings are worthy of further study.

Stress and the healthy adolescent brain: evidence for the neural embedding of life events.

Little is known about the long-term neural consequences of adverse life events for healthy adolescents, and this is particularly the case for events that occur after a putative stress-sensitive period in early childhood. In this functional magnetic resonance imaging study of healthy adolescents, we found that prior exposure to severe adverse life events was associated with current anxiety and with increased amygdala reactivity to standardized emotional stimuli (viewing of fearful faces relative to calm ones). Conjunction analyses identified multiple regions, including the amygdala, insula, and prefrontal cortex, in which reactivity to emotional faces covaried with life events as well as with current anxiety. Our morphometric analyses suggest systemic alterations in structural brain development with an association between anxiety symptoms and global gray matter volume. No life events were reported for the period before 4 years of age, suggesting that these results were not driven by exposure to stress during an early sensitive period in development. Overall, these data suggest systemic effects of traumatic events on the dynamically developing brain that are present even in a nonclinical sample of adolescents.

EARLY POSTPARTUM PARENTAL PREOCCUPATION AND POSITIVE PARENTING THOUGHTS: RELATIONSHIP WITH PARENT-INFANT INTERACTION.

Parenting behaviors and parent-infant emotional bonding during the early postpartum months play a critical role in infant development. However, the nature and progression of parental thoughts and their relationship with interactive behaviors have received less research. The current study investigated the trajectory of parental thoughts and behaviors among primiparous mothers (n = 18) and fathers (n = 15) and multiparous mothers (n = 13) and fathers (n = 13), which were measured at the first and third postpartum month. At the third postpartum month, the relationship between parental thoughts and parental interactive behaviors also was tested. Mothers and fathers showed high levels of preoccupations and caregiving thoughts during the first postpartum month that significantly declined by the third postpartum month. In contrast, positive thoughts about parenting and the infant increased over the same time interval. Mothers presented higher levels of preoccupations and positive thoughts than did fathers, and first-time parents reported more intense preoccupations than did experienced parents. Although maternal sensitivity was inversely related to maternal anxious thoughts, paternal sensitivity was predicted by higher levels of anxious as well as caregiving and positive thoughts.