Long-term cognitive sequelae of antenatal maternal anxiety: involvement of the orbitofrontal cortex

Anxiety and stress experienced by the mother during pregnancy are reported to have a negative association with the cognitive development of the child. An integration of recent evidence from cognitive reaction time tasks pointed to a deficit in endogenous response inhibition, a function ascribed to prefrontal cortex. To further delineate the cognitive sequelae associated with antenatal maternal anxiety, we reviewed recent neuro-imaging literature to create a cortical map of regions commonly and selectively activated by well-known cognitive tasks. The pragmatic value of this cortical map was tested in a follow-up sample of 49 17-year old adolescents. Adolescents of mothers with high levels of anxiety during week 12-22 of their pregnancy performed significantly lower in tasks which required integration and control of different task parameters. Working memory, inhibition of a prepotent response, and visual orienting of attention were not impaired. Based on the established cortical map, these results were related to subtle developmental aberrations in a part of, or in cortical and sub-cortical regions linked to, the orbitofrontal cortex.

[1]  R. Shalev,et al.  Sustained attention, activation and MPH in ADHD: a research note. , 1995, Journal of child psychology and psychiatry, and allied disciplines.

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

[3]  P. Viviani,et al.  Internally driven vs. externally cued movement selection: a study on the timing of brain activity. , 2000, Brain research. Cognitive brain research.

[4]  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.

[5]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[6]  S. Alborzian,et al.  Localized Orbitofrontal and Subcortical Metabolic Changes and Predictors of Response to Paroxetine Treatment in Obsessive-Compulsive Disorder , 1999, Neuropsychopharmacology.

[7]  Bill Faw.  Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: A tutorial review , 2003, Consciousness and Cognition.

[8]  Mariko Osaka,et al.  Cooperation of the anterior cingulate cortex and dorsolateral prefrontal cortex for attention shifting , 2004, NeuroImage.

[9]  J. Halperin,et al.  Sustained attention and response inhibition in young children at risk for Attention Deficit/Hyperactivity Disorder. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[10]  D. V. von Cramon,et al.  Localization of Executive Functions in Dual-Task Performance with fMRI , 2002, Journal of Cognitive Neuroscience.

[11]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[12]  J. Bartha,et al.  Maternal anxiety and fetal behavior at 15 weeks' gestation , 2003, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

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

[14]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[15]  R. Elliott,et al.  Response inhibition and impulsivity: an fMRI study , 2003, Neuropsychologia.

[16]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[17]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[18]  C D Frith,et al.  Functional Anatomy of Obsessive–Compulsive Phenomena , 1994, British Journal of Psychiatry.

[19]  H Garavan,et al.  A midline dissociation between error-processing and response-conflict monitoring , 2003, NeuroImage.

[20]  G. Gottlieb,et al.  A relational view of causality in normal and abnormal development , 2002, Development and Psychopathology.

[21]  G. Bohlin,et al.  Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[22]  M. Herrmann,et al.  Reduced response-inhibition in obsessive–compulsive disorder measured with topographic evoked potential mapping , 2003, Psychiatry Research.

[23]  T. Robbins,et al.  Decision-making processes following damage to the prefrontal cortex. , 2002, Brain : a journal of neurology.

[24]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[25]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[26]  J. Heron,et al.  Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. , 2002, The British journal of psychiatry : the journal of mental science.

[27]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[28]  J. Buitelaar,et al.  Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility? , 2004, Psychological bulletin.

[29]  J. Fuster.  The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[30]  D. V. van Essen,et al.  Windows on the brain: the emerging role of atlases and databases in neuroscience , 2002, Current Opinion in Neurobiology.

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

[32]  J. Prickaerts,et al.  Prenatal stress and neonatal rat brain development , 2006, Neuroscience.

[33]  James H. Johnson,et al.  The Test of Everyday Attention for Children (TEA-Ch): Patterns of Performance in Children With ADHD and Clinical Controls , 2001, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

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

[35]  P. Wadhwa.  Psychoneuroendocrine processes in human pregnancy influence fetal development and health , 2005, Psychoneuroendocrinology.

[36]  P. Gluckman,et al.  Living with the Past: Evolution, Development, and Patterns of Disease , 2004, Science.

[37]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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

[39]  Roy P. Martin,et al.  Prediction of Early Childhood Negative Emotionality and Inhibition from Maternal Distress during Pregnancy. , 1999 .

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

[41]  Y. Suh,et al.  Postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation, and synaptic protein expression , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[42]  T. O'Connor,et al.  Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[43]  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.

[44]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[45]  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.

[46]  C. Garel,et al.  MRI of the fetal brain : normal development and cerebral pathologies , 2004 .

[47]  A. Marcoen,et al.  High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. , 2004, Child development.

[48]  John J. Foxe,et al.  Prefrontal‐subcortical dissociations underlying inhibitory control revealed by event‐related fMRI , 2004, The European journal of neuroscience.

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

[50]  J. Grafman,et al.  Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. , 2003, Cerebral cortex.

[51]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[52]  E T Rolls,et al.  Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. , 2004, Brain : a journal of neurology.

[53]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[54]  H. Niederhofer,et al.  Prenatal Maternal Stress, Prenatal Fetal Movements and Perinatal Temperament Factors Influence Behavior and School Marks at the Age of 6 Years , 2004, Fetal Diagnosis and Therapy.

[55]  E. Rolls,et al.  Reward-related Reversal Learning after Surgical Excisions in Orbito-frontal or Dorsolateral Prefrontal Cortex in Humans , 2004, Journal of Cognitive Neuroscience.

[56]  A. Nobre,et al.  Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts , 2000, Neuropsychologia.

[57]  W. Fessner,et al.  Biocatalytic synthesis of hydroxylated natural products using aldolases and related enzymes. , 2001, Current opinion in biotechnology.

[58]  Ian H. Robertson,et al.  The test of everyday attention , 1994 .

[59]  Mark H. Johnson.  Brain development and cognition : a reader , 1993 .

[60]  Jan Theeuwes,et al.  Endogenous and exogenous attention shifts are mediated by the same large-scale neural network , 2004, NeuroImage.

[61]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[62]  S. Otte,et al.  Experience effects on brain development: possible contributions to psychopathology. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[63]  M. Rutter,et al.  Genetics and child psychiatry: I Advances in quantitative and molecular genetics. , 1999, Journal of child psychology and psychiatry, and allied disciplines.

[64]  M. Kringelbach.  The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[65]  Thomas E. Nichols,et al.  Switching attention and resolving interference: fMRI measures of executive functions , 2003, Neuropsychologia.