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

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.

[1]  L. Mayes,et al.  Disruption of Maternal Parenting Circuitry by Addictive Process: Rewiring of Reward and Stress Systems , 2011, Front. Psychiatry.

[2]  Samuel Asensio,et al.  Altered neural response of the appetitive emotional system in cocaine addiction: an fMRI Study , 2010, Addiction biology.

[3]  J. Weber,et al.  Prefrontal–striatal pathway underlies cognitive regulation of craving , 2010, Proceedings of the National Academy of Sciences.

[4]  L. Mayes,et al.  Problematic dyadic interaction among toddlers and their polydrug-cocaine-using mothers. , 2010, Infant mental health journal.

[5]  Peter Fonagy,et al.  What's in a Smile? Maternal Brain Responses to Infant Facial Cues , 2008, Pediatrics.

[6]  L. Mayes,et al.  THE MOTHERS AND TODDLERS PROGRAM: Preliminary Findings From an Attachment-Based Parenting Intervention for Substance-Abusing Mothers. , 2008, Psychoanalytic psychology : the official journal of the Division of Psychoanalysis, American Psychological Association, Division 39.

[7]  W. Bickel,et al.  A scale-free systems theory of motivation and addiction , 2007, Neuroscience & Biobehavioral Reviews.

[8]  L. Leavitt,et al.  Maternal sensory sensitivity, mother-infant 9-month interaction, infant attachment status: predictors of mother-toddler interaction at 24 months. , 2007, Infant behavior & development.

[9]  Samet Kose,et al.  Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[10]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[11]  P. Skudlarski,et al.  Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study , 2005, Psychopharmacology.

[12]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[13]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[14]  N. Volkow,et al.  Drug addiction: the neurobiology of behaviour gone awry , 2004, Nature Reviews Neuroscience.

[15]  E. Leibenluft,et al.  Mothers' neural activation in response to pictures of their children and other children , 2004, Biological Psychiatry.

[16]  J. Leckman,et al.  The development of parent-infant attachment through dynamic and interactive signaling loops of care and cry , 2004, Behavioral and Brain Sciences.

[17]  Yul-Wan Sung,et al.  Functional magnetic resonance imaging , 2004, Scholarpedia.

[18]  Andreas Bartels,et al.  The neural correlates of maternal and romantic love , 2004, NeuroImage.

[19]  Eric E. Nelson,et al.  Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants , 2004, NeuroImage.

[20]  Erich Seifritz,et al.  Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents , 2003, Biological Psychiatry.

[21]  J. Anthony,et al.  Maternal Cocaine Use: Estimated Effects on Mother-Child Play Interactions in the Preschool Period , 2002, Journal of developmental and behavioral pediatrics : JDBP.

[22]  David C. Alsop,et al.  Brain Activation during Facial Emotion Processing , 2002, NeuroImage.

[23]  Mark S. George,et al.  A potential role for thalamocingulate circuitry in human maternal behavior , 2002, Biological Psychiatry.

[24]  S. Luthar,et al.  The Mediating Role of Parenting Stress in Methadone-Maintained Mothers' Parenting , 2001, Parenting, science and practice.

[25]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[26]  J. Belsky,et al.  Child Care and Mother-Child Interaction in the First Three Years of Life , 1999 .

[27]  S J Kelley,et al.  Stress and coping behaviors of substance-abusing mothers. , 1998, Journal of the Society of Pediatric Nurses : JSPN.

[28]  M. Bornstein,et al.  The effects of polydrug use with and without cocaine on mother-infant interaction at 3 and 6 months , 1997 .

[29]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[30]  S. Thurman,et al.  The Effects of Prenatal Cocaine Exposure on Mother--Infant Interaction and Infant Arousal in the Newborn Period , 1994 .

[31]  L Murray,et al.  The impact of postnatal depression on infant development. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

[32]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[33]  G. Gustafson,et al.  Individual recognition of human infants on the basis of cries alone. , 1983, Developmental psychobiology.

[34]  M. Bornstein.  Handbook of Parenting , 2002 .

[35]  J C Gore,et al.  Functional magnetic resonance imaging of cocaine craving. , 2001, The American journal of psychiatry.

[36]  M. Reivich,et al.  Limbic activation during cue-induced cocaine craving. , 1999, The American journal of psychiatry.

[37]  P F Renshaw,et al.  Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. , 1998, The American journal of psychiatry.

[38]  L. Mayes,et al.  Substance abuse and parenting. , 1995 .