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

Neuropsychopharmacology (2011) 36, 2603–2615 & 2011 American College of Neuropsychopharmacology. All rights reserved 0893-133X/11 www.neuropsychopharmacology.org Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers Shir Atzil1,2, Talma Hendler2,3 and Ruth Feldman*,1 1 Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan, Israel; 2Functional Brain Center, Wohl Institute for Advanced Imaging, Tel-Aviv Sourasky Medical Center, Tel Aviv, Israel; 3Departments of Psychology and Physiology, Tel Aviv University, Tel Aviv, Israel 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 synchronyFthe coordination of maternal behavior with infant signalsFand intrusivenessFthe excessive expression of maternal behaviorFdescribe 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. Neuropsychopharmacology (2011) 36, 2603–2615; doi:10.1038/npp.2011.172; published online 31 August 2011 Keywords: maternal behavior; attachment; synchrony; imaging; motivation; emotion regulation INTRODUCTION The mother’s attachment to her infant is a complex process involving biological, behavioral, and psychological components that aim to ensure reproductive success and provide the foundation for the infant’s well-being and adaptation *Correspondence: Dr R Feldman, Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan 52900, Israel, Tel: + 972 3 5317943, Fax: + 972 3 535 0267, E-mail: Received 5 May 2011; revised 14 July 2011; accepted 21 July 2011 (Bowlby, 1958; Carter et al, 2005). Across mammalian species, infant growth and survival depend on the provision of a unique set of maternal behaviors that appear immediately after birth and function to organize the infant’s physiology and behavior (Leckman and Herman, 2002; Meaney, 2001). In humans, the maternal behavioral repertoire includes gaze at infant face, ‘motherese’ highpitched vocalizations, expression of positive affect, affectionate touch, and the synchronous adaptation of these behaviors to moments of infant responsiveness (Barrett and Fleming, 2011; Feldman and Eidelman, 2007). Such human maternal behaviors parallel the licking-and-grooming and Neurobiological basis of maternal attachment S Atzil et al 2604 arched-back nursing of other mammals, which have been linked with the affiliation-related neuropeptide Oxytocin and the functioning of motivational and affective neural systems (Champagne et al, 2004; Lee et al, 2000; Oxley and Fleming, 2000; Shahrokh et al, 2010; Strathearn et al, 2009; Toscano et al, 2009). However, to date, little research examined the integration of brain circuits, affiliative hormones, and maternal behavior in human mothers. The formation of the mother–infant bond draws on the timely provision of well-adapted maternal behaviors during the early post-partum period (Bowlby, 1969; Feldman et al, 2009; Tronick, 1989). Research in rodents indicates that naturally occurring variations in maternal behavior chart distinct patterns of mothering each associated with a specific bio-behavioral profile in mother and child. These patterns of maternal care initiate a cascade of epigenetic processes that uniquely shape gene expression, organize the Oxytocinergic system that supports bond formation in mammals, and determine the infant’s lifetime capacity to handle stress (Champagne, 2008; Weaver et al, 2004). Studies in humans have similarly shown that optimal mothering involves the synchronous coordination between maternal behavior and the infant’s social readiness (Feldman, 2007), and that the degree of interactive synchrony is associated with peripheral measures of Oxytocin in both parent and child (Feldman et al, 2010b, 2011). On the other hand, intrusive mothering describes a pattern of care that correlates with maternal anxiety and is expressed in excessive maternal behavior that disregards the child’s communications and provides stimulation when the infant signals a need for rest (Kaitz and Maytal, 2005). The human synchronous and intrusive maternal styles, like patterns of maternal care observed in other mammals, are naturally expressed variations in the general population and represent distinct bio-behavioral profiles of parenting. Longitudinal studies have shown that the synchronous and intrusive maternal constellations are individually stable from birth to adolescence, are associated with distinct patterns of maternal and infant HPA and parasympathetic response, and (...truncated)