The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period.

Animal studies suggest that structural changes occur in the maternal brain during the early postpartum period in regions such as the hypothalamus, amygdala, parietal lobe, and prefrontal cortex and such changes are related to the expression of maternal behaviors. In an attempt to explore this in humans, we conducted a prospective longitudinal study to examine gray matter changes using voxel-based morphometry on high resolution magnetic resonance images of mothers' brains at two time points: 2-4 weeks postpartum and 3-4 months postpartum. Comparing gray matter volumes across these two time points, we found increases in gray matter volume of the prefrontal cortex, parietal lobes, and midbrain areas. Increased gray matter volume in the midbrain including the hypothalamus, substantia nigra, and amygdala was associated with maternal positive perception of her baby. These results suggest that the first months of motherhood in humans are accompanied by structural changes in brain regions implicated in maternal motivation and behaviors.

[1]  P. Fonagy,et al.  Adult attachment predicts maternal brain and oxytocin response to infant cues , 2009, Neuropsychopharmacology.

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

[3]  K. Karelina,et al.  Motherhood Induces and Maintains Behavioral and Neural Plasticity across the Lifespan in the Rat , 2008, Archives of sexual behavior.

[4]  Gordon W. Gifford,et al.  Motherhood improves learning and memory , 1999, Nature.

[5]  E. Cadenas,et al.  Physiology and Neurobiology of Stress and Adaptation: Central Role of the Brain , 2007 .

[6]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

[7]  G. Mason,et al.  Oxytocin Activation of Maternal Behavior in the Rat a , 1992, Annals of the New York Academy of Sciences.

[8]  Pilyoung Kim,et al.  Perceived quality of maternal care in childhood and structure and function of mothers' brain. , 2009, Developmental science.

[9]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[10]  J. Stern,et al.  Forebrain expression of c-fos due to active maternal behaviour in lactating rats , 1997, Neuroscience.

[11]  M. Bornstein Handbook of Parenting , 2019 .

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

[13]  則内 まどか The functional neuroanatomy of maternal love : mother's response to infant's attachment behaviors , 2008 .

[14]  D. Cohen,et al.  Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive‐compulsive disorder , 1999, Acta psychiatrica Scandinavica. Supplementum.

[15]  M. Meaney,et al.  Nongenomic transmission across generations of maternal behavior and stress responses in the rat. , 1999, Science.

[16]  R Todd Constable,et al.  Maternal brain response to own baby-cry is affected by cesarean section delivery. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[17]  M. Merzenich,et al.  Alterations of the cortical representation of the rat ventrum induced by nursing behavior , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  M. Bohus,et al.  A voxel-based morphometric MRI study in female patients with borderline personality disorder , 2003, NeuroImage.

[19]  M. Iacoboni,et al.  Neural basis of maternal communication and emotional expression processing during infant preverbal stage. , 2009, Cerebral cortex.

[20]  J. Castro-Fornieles,et al.  A cross-sectional and follow-up voxel-based morphometric MRI study in adolescent anorexia nervosa. , 2009, Journal of psychiatric research.

[21]  Bogdan Draganski,et al.  Training-induced structural changes in the adult human brain , 2008, Behavioural Brain Research.

[22]  T. Sheehan,et al.  Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats , 2001, Neuroscience.

[23]  A. Fleming,et al.  Plasticity in the maternal circuit: effects of experience and partum condition on brain astrocyte number in female rats. , 2000, Behavioral neuroscience.

[24]  AW Toga,et al.  Brain Structure and Obesity , 2009, NeuroImage.

[25]  David Silbersweig,et al.  Hippocampal structural changes across the menstrual cycle , 2008, Hippocampus.

[26]  E. Nestler,et al.  Molecular basis of long-term plasticity underlying addiction , 2001, Nature Reviews Neuroscience.

[27]  F. Champagne,et al.  Behavioral/systems/cognitive Variations in Nucleus Accumbens Dopamine Associated with Individual Differences in Maternal Behavior in the Rat , 2022 .

[28]  Alison S Fleming,et al.  Medial prefrontal cortex lesions in the female rat affect sexual and maternal behavior and their sequential organization. , 2007, Behavioral neuroscience.

[29]  T. Insel,et al.  The Neurobiology of Parental Behavior , 2003, Hormones, Brain, and Behavior.

[30]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[31]  Christian Büchel,et al.  Changes in Gray Matter Induced by Learning—Revisited , 2008, PloS one.

[32]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[33]  A. Fleming,et al.  Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. , 1996, Behavioral neuroscience.

[34]  D. Blanchard,et al.  Effects of septal-forebrain lesions on maternal aggression and maternal care. , 1986, Behavioral and neural biology.

[35]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[36]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[37]  J. Šterc,et al.  Maternal behaviour in septal rat females. , 1993, Physiological research.

[38]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[39]  A. Fleming,et al.  Effects of transections to the vomeronasal nerves or to the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats. , 1992, Behavioral and neural biology.

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

[41]  H. D. Steklis,et al.  A neural substrate for affiliative behavior in nonhuman primates. , 1976, Brain, behavior and evolution.

[42]  Eva Gilboa-Schechtman,et al.  Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[43]  Gary H. Glover,et al.  Resilience after 9/11: Multimodal neuroimaging evidence for stress-related change in the healthy adult brain , 2008, NeuroImage.

[44]  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.

[45]  L. Mayes Arousal Regulation, Emotional Flexibility, Medial Amygdala Function, and the Impact of Early Experience , 2006, Annals of the New York Academy of Sciences.