Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers

Department of Psychology and Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel.
Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology (Impact Factor: 7.05). 08/2011; 36(13):2603-15. DOI: 10.1038/npp.2011.172
Source: PubMed


The mother-infant bond provides the foundation for the infant's future mental health and adaptation and depends on the provision of species-typical maternal behaviors that are supported by neuroendocrine and motivation-affective neural systems. Animal research has demonstrated that natural variations in patterns of maternal care chart discrete profiles of maternal brain-behavior relationships that uniquely shape the infant's lifetime capacities for stress regulation and social affiliation. Such patterns of maternal care are mediated by the neuropeptide Oxytocin and by stress- and reward-related neural systems. Human studies have similarly shown that maternal synchrony--the coordination of maternal behavior with infant signals--and intrusiveness--the excessive expression of maternal behavior--describe distinct and stable maternal styles that bear long-term consequences for infant well-being. To integrate brain, hormones, and behavior in the study of maternal-infant bonding, we examined the fMRI responses of synchronous vs intrusive mothers to dynamic, ecologically valid infant videos and their correlations with plasma Oxytocin. In all, 23 mothers were videotaped at home interacting with their infants and plasma OT assayed. Sessions were micro-coded for synchrony and intrusiveness. Mothers were scanned while observing several own and standard infant-related vignettes. Synchronous mothers showed greater activations in the left nucleus accumbens (NAcc) and intrusive mothers exhibited higher activations in the right amygdala. Functional connectivity analysis revealed that among synchronous mothers, left NAcc and right amygdala were functionally correlated with emotion modulation, theory-of-mind, and empathy networks. Among intrusive mothers, left NAcc and right amygdala were functionally correlated with pro-action areas. Sorting points into neighborhood (SPIN) analysis demonstrated that in the synchronous group, left NAcc and right amygdala activations showed clearer organization across time, whereas among intrusive mothers, activations of these nuclei exhibited greater cross-time disorganization. Correlations between Oxytocin with left NAcc and right amygdala activations were found only in the synchronous group. Well-adapted parenting appears to be underlay by reward-related motivational mechanisms, temporal organization, and affiliation hormones, whereas anxious parenting is likely mediated by stress-related mechanisms and greater neural disorganization. Assessing the integration of motivation and social networks into unified neural activity that reflects variations in patterns of parental care may prove useful for the study of optimal vs high-risk parenting.

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    • "Mothers and fathers synchronized their brain response to their 4-month-old infant's video in areas of the mentalizing and mirror networks including the inferior frontal gyrus(IFG) and inferior parietal lobule(IPL) (Atzil et al., 2012), demonstrating brain-to-brain synchrony in these areas in survival-related contexts. Regions in mothers' social brain were activated in response to videos depicting mother-infant synchrony, and the mother's behavioral synchrony during interaction with her infant predicted her brain response to synchrony in others (Atzil et al., 2014). These studies suggest that brain mechanisms underpinning participation in social synchrony also support neural response to stimuli depicting synchrony in others, particularly to viewing vignettes high in social synchrony. "
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    ABSTRACT: The capacity to act collectively within groups has led to the survival and thriving of Homo sapiens. A central group collaboration mechanism is "social synchrony," the coordination of behavior during joint action among affiliative members, which intensifies under threat. Here, we tested brain response to vignettes depicting social synchrony among combat veterans trained for coordinated action and following life-threatening group experience, versus controls, as modulated by oxytocin (OT), a neuropeptide supporting social synchrony. Using a randomized, double-blind, within-subject design, 40 combat-trained and control male veterans underwent magnetoencephalography (MEG) twice following OT/placebo administration while viewing two social vignettes rated as highly synchronous: pleasant male social gathering and coordinated unit during combat. Both vignettes activated a wide response across the social brain in the alpha band; the combat scene triggered stronger activations. Importantly, OT effects were modulated by prior experience. Among combat veterans, OT attenuated the increased response to combat stimuli in the posterior superior temporal sulcus (pSTS)- a hub of social perception, action observation, and mentalizing - and enhanced activation in the inferior parietal lobule (IPL) to the pleasant social scene. Among controls, OT enhanced inferior frontal gyrus (IFG) response to combat cues, demonstrating selective OT effects on mirror-neuron and mentalizing networks. OT-enhanced mirror network activity was dampened in veterans reporting higher posttraumatic symptoms. Results demonstrate that the social brain responds online, via modulation of alpha rhythms, to stimuli probing social synchrony, particularly those involving threat to survival, and OT's enhancing versus anxiolytic effects are sensitive to salient experiences within social groups.
    NeuroImage 10/2015; 124. DOI:10.1016/j.neuroimage.2015.09.066 · 6.36 Impact Factor
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    • "Maternal depression has also been associated with reduced/altered connectivity, expressed as decoupling of typical connectivity patterns such as between the amygdala and PCC (Chase et al., 2014), which suggests limitations on plasticity. Maternal depression has been repeatedly associated with diminished sensitivity and synchrony and activation in these areas is linked with increased maternal sensitivity and synchrony during mother–infant interactions (Atzil et al., 2011; Feldman, 2015b; Swain et al., 2007; Strathearn et al., 2009). With regards to maternal trauma or heightened maternal anxiety, some studies showed elevated amygdala activations (Schechter et al., 2012) whereas others found blunted amygdala activation (Kim et al., 2014a, 2014b). "
    Hormones and Behavior 09/2015; · 4.63 Impact Factor
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    • "Several exciting studies have now demonstrated that individual differences in parenting behaviors may be based on variations in neural responses to infant stimuli. In one of these studies, mothers at four to six months postpartum were divided into two groups: mothers with high synchronous scores and low intrusiveness scores (synchronous mothers) and mothers with low synchronous scores and high intrusiveness scores (intrusive mothers) (Atzil et al., 2011). Synchronous maternal behaviors, including coordination of gaze, touch, and vocalizations with infants, are interpreted as more sensitive parenting behaviors and are associated with positive infant outcomes. "
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    ABSTRACT: 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. Copyright © 2015. Published by Elsevier Inc.
    Hormones and Behavior 08/2015; DOI:10.1016/j.yhbeh.2015.08.001 · 4.63 Impact Factor
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