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      Maternal Neural Responses to Infant Cries and Faces: Relationships with Substance Use

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          Abstract

          Substance abuse in pregnant and recently post-partum women is a major public health concern because of effects on the infant and on the ability of the adult to care for the infant. In addition to the negative health effects of teratogenic substances on fetal development, substance use can contribute to difficulties associated with the social and behavioral aspects of parenting. Neural circuits associated with parenting behavior overlap with circuits involved in addiction (e.g., frontal, striatal, and limbic systems) and thus may be co-opted for the craving/reward cycle associated with substance use and abuse and be less available for parenting. The current study investigates the degree to which neural circuits associated with parenting are disrupted in mothers who are substance-using. Specifically, we used functional magnetic resonance imaging to examine the neural response to emotional infant cues (faces and cries) in substance-using compared to non-using mothers. In response to both faces (of varying emotional valence) and cries (of varying distress levels), substance-using mothers evidenced reduced neural activation in regions that have been previously implicated in reward and motivation as well as regions involved in cognitive control. Specifically, in response to faces, substance users showed reduced activation in prefrontal regions, including the dorsolateral and ventromedial prefrontal cortices, as well as visual processing (occipital lobes) and limbic regions (parahippocampus and amygdala). Similarly, in response to infant cries, substance-using mothers showed reduced activation relative to non-using mothers in prefrontal regions, auditory sensory processing regions, insula and limbic regions (parahippocampus and amygdala). These findings suggest that infant stimuli may be less salient for substance-using mothers, and such reduced saliency may impair developing infant-caregiver attachment and the ability of mothers to respond appropriately to their infants.

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            The neural correlates of maternal and romantic love.

            Romantic and maternal love are highly rewarding experiences. Both are linked to the perpetuation of the species and therefore have a closely linked biological function of crucial evolutionary importance. Yet almost nothing is known about their neural correlates in the human. We therefore used fMRI to measure brain activity in mothers while they viewed pictures of their own and of acquainted children, and of their best friend and of acquainted adults as additional controls. The activity specific to maternal attachment was compared to that associated to romantic love described in our earlier study and to the distribution of attachment-mediating neurohormones established by other studies. Both types of attachment activated regions specific to each, as well as overlapping regions in the brain's reward system that coincide with areas rich in oxytocin and vasopressin receptors. Both deactivated a common set of regions associated with negative emotions, social judgment and 'mentalizing', that is, the assessment of other people's intentions and emotions. We conclude that human attachment employs a push-pull mechanism that overcomes social distance by deactivating networks used for critical social assessment and negative emotions, while it bonds individuals through the involvement of the reward circuitry, explaining the power of love to motivate and exhilarate.
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              Prefrontal-striatal pathway underlies cognitive regulation of craving.

              The ability to control craving for substances that offer immediate rewards but whose long-term consumption may pose serious risks lies at the root of substance use disorders and is critical for mental and physical health. Despite its importance, the neural systems supporting this ability remain unclear. Here, we investigated this issue using functional imaging to examine neural activity in cigarette smokers, the most prevalent substance-dependent population in the United States, as they used cognitive strategies to regulate craving for cigarettes and food. We found that the cognitive down-regulation of craving was associated with (i) activity in regions previously associated with regulating emotion in particular and cognitive control in general, including dorsomedial, dorsolateral, and ventrolateral prefrontal cortices, and (ii) decreased activity in regions previously associated with craving, including the ventral striatum, subgenual cingulate, amygdala, and ventral tegmental area. Decreases in craving correlated with decreases in ventral striatum activity and increases in dorsolateral prefrontal cortex activity, with ventral striatal activity fully mediating the relationship between lateral prefrontal cortex and reported craving. These results provide insight into the mechanisms that enable cognitive strategies to effectively regulate craving, suggesting that it involves neural dynamics parallel to those involved in regulating other emotions. In so doing, this study provides a methodological tool and conceptual foundation for studying this ability across substance using populations and developing more effective treatments for substance use disorders.
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                Author and article information

                Journal
                Front Psychiatry
                Front. Psychiatry
                Frontiers in Psychiatry
                Frontiers Research Foundation
                1664-0640
                12 April 2011
                15 June 2011
                2011
                : 2
                : 32
                Affiliations
                [1] 1simpleYale Child Study Center, Yale University School of Medicine New Haven, CT, USA
                [2] 2simpleHaskins Laboratories New Haven, CT, USA
                [3] 3simpleDepartment of Psychiatry, Yale University School of Medicine New Haven, CT, USA
                [4] 4simpleDepartment of Neurobiology, Yale University School of Medicine New Haven, CT, USA
                Author notes

                Edited by: Rina Eiden, University at Buffalo, USA

                Reviewed by: Eamon McCrory, University College London, UK; Andrew James Gerber, Columbia University, USA

                *Correspondence: Nicole Landi, E 74 Yale Child Study Center, 230 South Frontage Road, New Haven, CT 06511, USA. e-mail: nicole.landi@ 123456yale.edu

                This article was submitted to Frontiers in Child and Neurodevelopmental Psychiatry, a aspecialty of Frontiers in Psychiatry.

                Article
                10.3389/fpsyt.2011.00032
                3118477
                21720537
                6c63b6ba-bacb-4dd2-9967-32e870d06623
                Copyright © 2011 Landi, Montoya, Kober, Rutherford, Mencl, Worhunsky, Potenza and Mayes.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 03 March 2011
                : 22 May 2011
                Page count
                Figures: 2, Tables: 7, Equations: 0, References: 42, Pages: 13, Words: 9310
                Categories
                Psychiatry
                Original Research

                Clinical Psychology & Psychiatry
                emotion,fmri,parenting,cry
                Clinical Psychology & Psychiatry
                emotion, fmri, parenting, cry

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