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.

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.

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.

Trait coping styles and the maternal neural and behavioral sensitivity to an infant.

During the postpartum period, new mothers experience drastic changes in their body, brain, and life circumstances. Stress from the emotional and physical demands of caring for an infant is associated with negative mood and parenting outcomes. The use of active coping strategies can increase mothers' resilience during the postpartum period. However, little is known about the association between coping styles and maternal brain responses to infant cues. In the current study, we examined the associations among trait coping style, maternal brain responses, and behavioral sensitivity in a socioeconomically diverse sample of first-time mothers (N = 59). The use of more active trait coping strategies compared to passive coping strategies was associated with increased brain responses to infant cry sounds in brain regions that are critically involved in motivation and emotion regulation-substantia nigra, anterior cingulate gyrus, and inferior frontal gyrus. Increased brain activations in the midbrain and anterior cingulate gyrus were further associated with higher levels of maternal sensitivity observed during interactions with the infant. Thus, the findings provide support for mothers' use of more active coping styles to promote neural and behavioral resilience for a positive transition to parenthood.

Reported maternal childhood maltreatment experiences, amygdala activation and functional connectivity to infant cry.

Maternal childhood maltreatment experiences (CMEs) may influence responses to infants and affect child outcomes. We examined associations between CME and mothers' neural responses and functional connectivity to infant distress. We hypothesized that mothers with greater CME would exhibit higher amygdala reactivity and amygdala-supplementary motor area (SMA) functional connectivity to own infant's cries. Postpartum mothers (N = 57) assessed for CME completed an functional magnetic resonance imaging task with cry and white-noise stimuli. Amygdala region-of-interest and psychophysiological interaction analyses were performed. Our models tested associations of CME with activation and connectivity during task conditions (own/other and cry/noise). Exploratory analyses with parenting behaviors were performed. Mothers with higher CME exhibited higher amygdala activation to own baby's cries vs other stimuli (F1,392 = 6.9, P < 0.01, N = 57) and higher differential connectivity to cry vs noise between amygdala and SMA (F1,165 = 22.3, P < 0.001). Exploratory analyses revealed positive associations between both amygdala activation and connectivity and maternal non-intrusiveness (Ps < 0.05). Increased amygdala activation to own infant's cry and higher amygdala-SMA functional connectivity suggest motor responses to baby's distress. These findings were associated with less intrusive maternal behaviors. Follow-up studies might replicate these findings, add more granular parenting assessments and explore how cue processing leads to a motivated maternal approach in clinical populations.

Neural processing of infant and adult face emotion and maternal exposure to childhood maltreatment.

Face processing in mothers is linked to mother-infant social communication, which is critical for parenting and in turn for child development. Neuroimaging studies of child maltreatment-exposed (CME) mothers are sparse compared to studies of mothers with postpartum depression, which have suggested blunted amygdala reactivity to infant stimuli. We expected to see a similar pattern in CME mothers. Based on broader studies in trauma-exposed populations, we anticipated increased amygdala reactivity to negative adult face stimuli in a comparison task in CME mothers given heightened evaluation of potential threat. We examined Neuroimaging studies of mothers with childhood maltreatment exposure (CME) (18-37 years old), who performed infant (N = 45) and/or adult (N = 46) face processing tasks. CME mothers exhibited blunted bilateral amygdala reactivity to infant faces. There was no between-group difference in amygdala reactivity to adult faces. In infant and adult face processing tasks regardless of CME, superior temporal gyrus activation was increased for negative-valence stimuli. Our preliminary findings suggest that childhood maltreatment alters maternal processing of infant social cues, a critical skill impacting infant socioemotional development.

Cortical thickness variation of the maternal brain in the first 6 months postpartum: associations with parental self-efficacy.

The postpartum period is associated with structural and functional plasticity in brain regions involved in parenting. While one study identified an increase in gray matter volume during the first 4 months among new mothers, little is known regarding the relationship between cortical thickness across postpartum months and perceived adjustment to parenthood. In this study of 39 socioeconomically diverse first-time new mothers, we examined the relations among postpartum months, cortical thickness, and parental self-efficacy. We identified a positive association between postpartum months and cortical thickness in the prefrontal cortex including the superior frontal gyrus extending into the medial frontal and orbitofrontal gyri, in the lateral occipital gyrus extending into the inferior parietal and fusiform gyri, as well as in the caudal middle frontal and precentral gyri. The relationship between cortical thickness and parental self-efficacy was specific to the prefrontal regions. These findings contribute to our understanding of the maternal brain in the first 6 months postpartum and provide evidence of a relationship between brain structure and perceived adjustment to parenthood.

The cortisol awakening response (CAR) in toddlers: Nap-dependent effects on the diurnal secretory pattern.

INTRODUCTION: Cortisol levels in adults show a sharp decrease from mid-morning to mid-afternoon. Most toddlers take afternoon naps, which is associated with a less mature diurnal pattern characterized by a midday plateau in cortisol secretion. Napping in preschoolers produces a robust cortisol awakening response (CAR), which may account for such maturational differences. This experimental study extends prior work by examining whether the presence and timing of the nap-dependent CAR influences the diurnal cortisol pattern in toddlers. METHODS: Toddlers (n = 28; 13 females; 30-36 months) followed a strict biphasic sleep schedule (≥ 12.5h time in bed; ≥ 90 min nap) for ≥ 3 days before each of four randomly ordered, in-home cortisol assessments. For each assessment, saliva samples were obtained at morning awakening, ∼ 09:30, pre-nap, 0, 15, 30, 45, 90, and 135 min post-nap awakening (verified with actigraphy), and ∼ 19:30. On one day, children napped at their scheduled time, and parents collected saliva samples. On another day, children missed their nap, and parents collected saliva samples at matched times. On two other days, children napped 4h (morning) and 7h (afternoon) after awakening in the morning, during which time researchers collected pre- and post-nap saliva samples. Saliva was assayed for cortisol (µg/dl). RESULTS: Three-level multilevel models were used to estimate the CAR and diurnal cortisol patterns in all four conditions. Compared to the no-nap condition (no observed CAR; b = -0.78, p = 0.65), we found a pronounced cortisol rise following the morning nap (b = 11.00, p < 0.001) and both afternoon naps whether samples were collected by parents (b = 5.19, p < 0.01) or experimenters (b = 4.97, p < 0.01). Napping in the morning resulted in the most robust post-nap cortisol rise (b = 10.21, p < 0.001). Diurnal patterns were analyzed using piecewise growth modeling that estimated linear coefficients for five separate periods throughout the day (corresponding to morning decline, noon decline, post-nap rise, post-nap decline, and evening decline). We observed a significant post-nap rise in cortisol values on the parent-collected afternoon nap (b = 3.41, p < 0.01) and the experimenter-collected morning nap (b = 7.50, p < 0.01) days as compared to the no-nap day (b = -0.17, p = 0.82). No other differences in diurnal profiles were observed between the parent-collected nap and no-nap conditions; however, toddlers had a steeper evening decline on the day of the morning nap compared to the parent-collected afternoon nap (b = 0.30, p < 0.05) and no-nap conditions (b = 0.27, p < 0.05). DISCUSSION: These well-controlled findings suggest that the presence and timing of daytime naps influence the pattern of diurnal cortisol secretion in toddlers. They also provide support for the hypothesis that napping is the primary state driving the immature midday plateau in cortisol secretion, which becomes more adult-like across childhood. Prior studies of the diurnal cortisol pattern have employed a cubic model, and therefore, have not detected all possible variations due to napping. Our experimental data have important methodological implications for researchers examining associations between the slope of the diurnal cortisol pattern and developmental outcomes, as well as those utilizing afternoon cortisol reactivity protocols in napping children.