Maternal Neural Reactivity During Pregnancy Predicts Infant Temperament.

Maternal biological systems impact infant temperament as early as the prenatal period, though the mechanisms of this association are unknown. Using a prospective, longitudinal design, we found that maternal (N = 89) amplitudes of the late positive potential (LPP) in response to negative stimuli during the second, but not the third, trimester of pregnancy predicted observed and physiological indices of temperamental reactivity in infants at age 4 months. Maternal LPP was positively associated with observed infant fear and negatively associated with frontal EEG asymmetry and cortisol reactivity in infants at age 4 months. Results identify a putative mechanism, early in pregnancy, for the intergenerational transmission of emotional reactivity from mother to infant.

[1]  R. Kotov,et al.  Diagnostic and Symptom-Based Predictors of Emotional Processing in Generalized Anxiety Disorder and Major Depressive Disorder: An Event-Related Potential Study , 2016, Cognitive Therapy and Research.

[2]  J. Li,et al.  Effects of Maternal Cortisol during Pregnancy on Children's Blood Pressure Responses , 2015, Neuroendocrinology.

[3]  J. Banks,et al.  Acute Stress Dysregulates the LPP ERP Response to Emotional Pictures and Impairs Sustained Attention: Time-Sensitive Effects , 2015, Brain sciences.

[4]  P. Gluckman,et al.  Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants , 2015, Translational Psychiatry.

[5]  R. Davidson,et al.  The development of stranger fear in infancy and toddlerhood: normative development, individual differences, antecedents, and outcomes. , 2013, Developmental science.

[6]  E. Davis,et al.  Dysregulated Fear Predicts Social Wariness and Social Anxiety Symptoms during Kindergarten , 2013, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[7]  V. Glover,et al.  Prenatal maternal anxiety predicts reduced adaptive immunity in infants , 2013, Brain, Behavior, and Immunity.

[8]  D. Reiss,et al.  Measurement and associations of pregnancy risk factors with genetic influences, postnatal environmental influences, and toddler behavior , 2013, International journal of behavioral development.

[9]  Tim P. Moran,et al.  The psychometric properties of the late positive potential during emotion processing and regulation , 2013, Brain Research.

[10]  A. Keil,et al.  Neural Substrate of the Late Positive Potential in Emotional Processing , 2012, The Journal of Neuroscience.

[11]  J. Clauss,et al.  Behavioral inhibition and risk for developing social anxiety disorder: a meta-analytic study. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[12]  Martha Ann Bell,et al.  Using EEG to Study Cognitive Development: Issues and Practices , 2012, Journal of cognition and development : official journal of the Cognitive Development Society.

[13]  B. Shahbaba,et al.  Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems , 2012, Proceedings of the National Academy of Sciences.

[14]  E. Davis,et al.  Prenatal maternal anxiety and early childhood temperament , 2011, Stress.

[15]  S. Putnam Stability and instability of childhood traits: implications for personality development of animals. , 2011, Developmental psychobiology.

[16]  J. Deloache,et al.  Prefrontal Asymmetry and Parent-Rated Temperament in Infants , 2011, PloS one.

[17]  K. Buss,et al.  Toddlers' context-varying emotions, maternal responses to emotions, and internalizing behaviors. , 2011, Emotion.

[18]  Marco Del Giudice,et al.  The Adaptive Calibration Model of stress responsivity , 2011, Neuroscience & Biobehavioral Reviews.

[19]  K. Buss Which fearful toddlers should we worry about? Context, fear regulation, and anxiety risk. , 2011, Developmental psychology.

[20]  C. Buss,et al.  Prenatal Programming of Human Neurological Function , 2011, International journal of peptides.

[21]  S. Pawlby,et al.  Increased pituitary-adrenal activation and shortened gestation in a sample of depressed pregnant women: a pilot study. , 2011, Journal of affective disorders.

[22]  M. Kutner,et al.  Validity of depression rating scales during pregnancy and the postpartum period: impact of trimester and parity. , 2011, Journal of psychiatric research.

[23]  Ashley L. Hill-Soderlund,et al.  Fear and anger reactivity trajectories from 4 to 16 months: the roles of temperament, regulation, and maternal sensitivity. , 2010, Developmental psychology.

[24]  D. Klein,et al.  Temperamental Positive and Negative Emotionality and Children's Depressive Symptoms: A Longitudinal Prospective Study from Age Three to Age Ten , 2010 .

[25]  A. Chicz–DeMet,et al.  Attenuation of maternal psychophysiological stress responses and the maternal cortisol awakening response over the course of human pregnancy , 2010, Stress.

[26]  N. Fox,et al.  Temperament and the environment in the etiology of childhood anxiety. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[27]  G. Hajcak,et al.  Distinct electrocortical and behavioral evidence for increased attention to threat in generalized anxiety disorder , 2010, Depression and anxiety.

[28]  G. Hajcak,et al.  Event-Related Potentials, Emotion, and Emotion Regulation: An Integrative Review , 2010, Developmental neuropsychology.

[29]  C. Buss,et al.  High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children , 2010, Psychoneuroendocrinology.

[30]  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.

[31]  N. Fox,et al.  Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[32]  M. Gunnar,et al.  Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol , 2009, Psychoneuroendocrinology.

[33]  Dan Foti,et al.  Tell me about it: neural activity elicited by emotional pictures and preceding descriptions. , 2009, Emotion.

[34]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

[35]  Dan Foti,et al.  Deconstructing Reappraisal: Descriptions Preceding Arousing Pictures Modulate the Subsequent Neural Response , 2008, Journal of Cognitive Neuroscience.

[36]  A. Chicz–DeMet,et al.  Prenatal exposure to maternal depression and cortisol influences infant temperament. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[37]  J. Giedd,et al.  Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging , 2006, Neuroscience & Biobehavioral Reviews.

[38]  S. Nieuwenhuis,et al.  Reappraisal modulates the electrocortical response to unpleasant pictures , 2006, Cognitive, affective & behavioral neuroscience.

[39]  Sangmoon Kim,et al.  Depression, anxiety, and resting frontal EEG asymmetry: a meta-analytic review. , 2006, Journal of abnormal psychology.

[40]  J. Nigg,et al.  Temperament and developmental psychopathology. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[41]  E. Leerkes,et al.  Infant and maternal behavior moderate reactivity to novelty to predict anxious behavior at 2.5 years , 2006, Development and Psychopathology.

[42]  Vera Ferrari,et al.  Repetitive picture processing: Autonomic and cortical correlates , 2006, Brain Research.

[43]  Maarten Mennes,et al.  Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review , 2005, Neuroscience & Biobehavioral Reviews.

[44]  P. Wadhwa,et al.  Prenatal Maternal Anxiety and Depression Predict Negative Behavioral Reactivity in Infancy , 2004 .

[45]  E. Leerkes,et al.  Infant and maternal behaviors regulate infant reactivity to novelty at 6 months. , 2004, Developmental psychology.

[46]  John J. B. Allen,et al.  Issues and assumptions on the road from raw signals to metrics of frontal EEG asymmetry in emotion , 2004, Biological Psychology.

[47]  M. Rothbart,et al.  Studying infant temperament via the Revised Infant Behavior Questionnaire , 2003 .

[48]  J. DiPietro,et al.  Maternal stress and affect influence fetal neurobehavioral development. , 2002, Developmental psychology.

[49]  J. Gross Emotion regulation: affective, cognitive, and social consequences. , 2002, Psychophysiology.

[50]  C E Tenke,et al.  Event-related potentials (ERPs) to hemifield presentations of emotional stimuli: differences between depressed patients and healthy adults in P3 amplitude and asymmetry. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[52]  J. Kagan,et al.  Early childhood predictors of adult anxiety disorders , 1999, Biological Psychiatry.

[53]  Karin S. Frey,et al.  Frontal brain electrical activity in infants of depressed and nondepressed mothers: Relation to variations in infant behavior , 1999, Development and Psychopathology.

[54]  A. Chicz–DeMet,et al.  Maternal corticotropin-releasing hormone and habituation in the human fetus. , 1999, Developmental psychobiology.

[55]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[56]  E. Tronick,et al.  Emotional characteristics of infants associated with maternal depression and anxiety. , 1998, Pediatrics.

[57]  D J Barker,et al.  In utero programming of chronic disease. , 1998, Clinical science.

[58]  John J. B. Allen,et al.  Anger and frontal brain activity: EEG asymmetry consistent with approach motivation despite negative affective valence. , 1998, Journal of personality and social psychology.

[59]  J. Strelau Galen's prophecy: Temperament in human nature , 1998 .

[60]  S. Shelton,et al.  Individual differences in freezing and cortisol in infant and mother rhesus monkeys. , 1998, Behavioral neuroscience.

[61]  G A Miller,et al.  Patterns of regional brain activity differentiate types of anxiety. , 1997, Journal of abnormal psychology.

[62]  C. Nelson,et al.  Event-related potentials in year-old infants: relations with emotionality and cortisol. , 1994, Child development.

[63]  R. Davidson Anterior cerebral asymmetry and the nature of emotion , 1992, Brain and Cognition.

[64]  M. Gunnar Reactivity of the hypothalamic-pituitary-adrenocortical system to stressors in normal infants and children. , 1992, Pediatrics.

[65]  R. Kestenbaum,et al.  Infant proneness-to-distress temperament, maternal personality, and mother-infant attachment: associations and goodness of fit. , 1990, Child development.

[66]  N. Fox,et al.  Frontal brain asymmetry predicts infants' response to maternal separation. , 1989, Journal of abnormal psychology.

[67]  J. Cox,et al.  Detection of Postnatal Depression , 1987, British Journal of Psychiatry.

[68]  N. Fox,et al.  Electroencephalogram Asymmetry in Response to the Approach of a Stranger and Maternal Separation in 10-Month-Old Infants. , 1987 .

[69]  P. Cole Children's spontaneous control of facial expression. , 1986 .

[70]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[71]  Sabrina Eberhart,et al.  Applied Missing Data Analysis , 2016 .

[72]  H. Goldsmith,et al.  Behavioral assessment of temperament. , 2012 .

[73]  B. Peterson,et al.  Normal Development of Brain Circuits , 2010, Neuropsychopharmacology.

[74]  E. Davis,et al.  The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. , 2010, Child development.

[75]  J. Bates,et al.  Child Temperament: An Integrative Review of Concepts, Research Programs, and Measures , 2008 .

[76]  L. Schmidt Patterns of second-by-second resting frontal brain (EEG) asymmetry and their relation to heart rate and temperament in 9-month-old human infants , 2008 .

[77]  M. Gunnar,et al.  The neurobiology of stress and development. , 2007, Annual review of psychology.

[78]  A. Wenzel,et al.  Anxiety symptoms and disorders at eight weeks postpartum. , 2005, Journal of anxiety disorders.

[79]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[80]  J. Pickens,et al.  EEG Stability in Infants/Children of Depressed Mothers , 1997, Child psychiatry and human development.

[81]  T J Meyer,et al.  Development and validation of the Penn State Worry Questionnaire. , 1990, Behaviour research and therapy.

[82]  Sandra Smidt,et al.  Socioemotional development. , 1988, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[83]  H. Goldsmith,et al.  Toward a Theory of Infant Temperament , 1982 .

[84]  R. Harmon,et al.  The Development of Attachment and Affiliative Systems , 1982, Topics in Developmental Psychobiology.