Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety

OBJECTIVE To assess the association between maternal anxiety during pregnancy and the brain activity of 17 year old adolescents performing two cognitive control tasks. METHODS Twenty-three 17 year old boys of mothers whose level of anxiety was measured during pregnancy were investigated using ERP while performing a Go/Nogo paradigm assessing exogenous cognitive control and a Gambling paradigm requiring endogenous cognitive control. RESULTS No effects of antenatal maternal anxiety were observed in the Go/Nogo paradigm. However, in the Gambling paradigm adolescents of the high anxiety group (n=8) showed a less efficient pattern of decision making compared to the adolescents in the low-average anxiety group (n=15). Moreover, only for this task the ERP data showed an enlarged early frontal P2a component in the high anxiety group. CONCLUSIONS The brain activity of adolescents during an endogenous cognitive control task is associated to the level of anxiety experienced by their mother during pregnancy. This association was not observed during an exogenous cognitive control task. SIGNIFICANCE This study indicates that a child's brain functionality is related to its mother's anxiety during pregnancy. Endogenous cognitive control is regarded the cognitive function most affected by the level of antenatal maternal anxiety.

[1]  P. Zelazo,et al.  Stress During Pregnancy Affects General Intellectual and Language Functioning in Human Toddlers , 2004, Pediatric Research.

[2]  M. Brass,et al.  Decomposing Components of Task Preparation with Functional Magnetic Resonance Imaging , 2004, Journal of Cognitive Neuroscience.

[3]  D. Tucker,et al.  Frontal evaluation and posterior representation in target detection. , 2001, Brain research. Cognitive brain research.

[4]  Gilles Pourtois,et al.  Unavoidable errors: A spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task , 2008, Neuropsychologia.

[5]  Arturas Petronis,et al.  Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[6]  F. Guillem,et al.  Dissociating memory processes involved in direct and indirect tests with ERPs to unfamiliar faces. , 2001, Brain research. Cognitive brain research.

[7]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[8]  Tracy A. Dennis,et al.  Trait anxiety and conflict monitoring following threat: an ERP study. , 2009, Psychophysiology.

[9]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[10]  T. O'Connor,et al.  Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[11]  S. Huffel,et al.  Antenatal Maternal Anxiety is Related to HPA-Axis Dysregulation and Self-Reported Depressive Symptoms in Adolescence: A Prospective Study on the Fetal Origins of Depressed Mood , 2008, Neuropsychopharmacology.

[12]  J. Buitelaar,et al.  Does Maternal Prenatal Stress Adversely Affect the Child’s Learning and Memory at Age Six? , 2006, Journal of abnormal child psychology.

[13]  E. Bullmore,et al.  Mapping Motor Inhibition: Conjunctive Brain Activations across Different Versions of Go/No-Go and Stop Tasks , 2001, NeuroImage.

[14]  S. Luck,et al.  Electrophysiological correlates of feature analysis during visual search. , 1994, Psychophysiology.

[15]  L. Spear.  The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[16]  G. Potts.  An ERP index of task relevance evaluation of visual stimuli , 2004, Brain and Cognition.

[17]  Andrew D. Roberts,et al.  Sensory processing disorder in a primate model: evidence from a longitudinal study of prenatal alcohol and prenatal stress effects. , 2008, Child development.

[18]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[19]  Lieven Lagae,et al.  Long-term cognitive sequelae of antenatal maternal anxiety: involvement of the orbitofrontal cortex , 2006, Neuroscience & Biobehavioral Reviews.

[20]  Y. Ben-Shlomo,et al.  Prenatal Anxiety Predicts Individual Differences in Cortisol in Pre-Adolescent Children , 2005, Biological Psychiatry.

[21]  K. Konrad,et al.  Integrating genetic, psychopharmacological and neuroimaging studies: A converging methods approach to understanding the neurobiology of ADHD , 2007 .

[22]  L. Jonkman,et al.  The development of preparation, conflict monitoring and inhibition from early childhood to young adulthood; a Go/Nogo ERP study , 2006, Brain Research.

[23]  K. R. Ridderinkhof,et al.  Electrophysiological correlates of anterior cingulate function in a go/no-go task: Effects of response conflict and trial type frequency , 2003, Cognitive, affective & behavioral neuroscience.

[24]  J. Jonides,et al.  The mind's eye, looking inward? In search of executive control in internal attention shifting. , 2003, Psychophysiology.

[25]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[26]  P. B. Defares,et al.  Handleiding bij de Zelf-beoordelings Vragenlijst ZBV. Een nederlandstalige bewerking van de Spielberger State-Trait Anxiety Inventory , 1980 .

[27]  E. Gould,et al.  Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile Rhesus monkeys , 2003, Biological Psychiatry.

[28]  J. Nigg,et al.  Low Blood Lead Levels Associated with Clinically Diagnosed Attention-Deficit/Hyperactivity Disorder and Mediated by Weak Cognitive Control , 2008, Biological Psychiatry.

[29]  L. Lagae,et al.  High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds , 2005, Neuroscience & Biobehavioral Reviews.

[30]  Bruno Kopp,et al.  Temporal dynamics of selective attention and conflict resolution during cross-dimensional go-nogo decisions , 2007, BMC Neuroscience.

[31]  D. Glahn,et al.  Electrophysiological correlates of response inhibition in children and adolescents with ADHD: influence of gender, age, and previous treatment history. , 2007, Psychophysiology.

[32]  M J Taylor1,et al.  Top-down modulation of early selective attention processes in children. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  J. Polich,et al.  EEG and ERP assessment of normal aging. , 1997, Electroencephalography and clinical neurophysiology.

[34]  Lorna C. Quandt,et al.  Anxiety and error monitoring: Increased error sensitivity or altered expectations? , 2007, Brain and Cognition.

[35]  Lieven Lagae,et al.  ERP correlates of complex human decision making in a gambling paradigm: detection and resolution of conflict. , 2008, Psychophysiology.

[36]  R. Simons,et al.  The effects of fear on performance monitoring and attentional allocation. , 2005, Psychophysiology.

[37]  P. Gluckman,et al.  Early life events and their consequences for later disease: A life history and evolutionary perspective , 2007, American journal of human biology : the official journal of the Human Biology Council.

[38]  P. Nathanielsz.  Life in the Womb: The Origin of Health and Disease , 1999 .

[39]  T. Sejnowski,et al.  Functionally Independent Components of the Late Positive Event-Related Potential during Visual Spatial Attention , 1999, The Journal of Neuroscience.

[40]  T. Paus.  Mapping brain maturation and cognitive development during adolescence , 2005, Trends in Cognitive Sciences.

[41]  V. Pop,et al.  Maternal anxiety during pregnancy and subsequent infant development , 2001 .

[42]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[43]  F. Rice,et al.  The impact of gestational stress and prenatal growth on emotional problems in offspring: a review , 2007, Acta psychiatrica Scandinavica.

[44]  Fetal hypothalamic-pituitary-adrenal stress responses to invasive procedures are independent of maternal responses. , 2001, The Journal of clinical endocrinology and metabolism.

[45]  John J. Foxe,et al.  Task switching: a high-density electrical mapping study , 2003, NeuroImage.

[46]  P. Read Montague,et al.  When Things Are Better or Worse than Expected: The Medial Frontal Cortex and the Allocation of Processing Resources , 2006, Journal of Cognitive Neuroscience.

[47]  Lieven Lagae,et al.  ADHD Deficit as Measured in Adolescent Boys with a Continuous Performance Task Is Related to Antenatal Maternal Anxiety , 2006, Pediatric Research.