High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds
Introduction
Negative maternal emotional states during pregnancy have been shown to influence the development of the child to be born. The effects are observable prior to birth as well as in the neonate, infant and child (for a review, see [1], [2], [3], [4]). High maternal anxiety and stress during pregnancy are for instance associated with alterations in fetal motor activity and heart rate patterns (e.g. [5], [6], [7], [8], [9]) and with childhood disorders such as attention deficit hyperactivity disorder (ADHD), externalizing and internalizing behavior [10], [11], [12], [13], [14]. ADHD symptoms (inattention, hyperactivity, impulsivity), externalizing behavior (aggression, acting-out behavior) and internalizing behavior (anxiety, emotional inhibition and lability) may be seen as problems with regulation at the cognitive level (e.g. attention problems, impulsive cognitive style), behavioral level (e.g. hyperactivity) and emotional level (e.g. acting-out behavior, anxiety) (e.g. [15], [16]). In some studies the effects are only present when the negative maternal state occurs relatively early in the pregnancy. For instance, Van den Bergh and Marcoen [14] found an association between high anxiety at 12–22 weeks of pregnancy and ADHD symptoms, externalizing problems, and self-report anxiety in 8–9-year-old children, and did not find this association for high anxiety occurring later in gestation. In contrast, in the study of O'Connor et al. [11], [12] the strongest effects were found for late gestation periods.
It is not known at present how maternal emotional states can induce these behavioral effects. Most likely, anxiety and stress related hormones originating from the mother play a crucial role. These hormones can enter the fetal organism [17], and if present during specific sensitive developmental periods, they are thought to disturb the programming of certain biological systems responsible for the regulation of fetal and later behavior [18], [19], [20], [21], [22], [23]. For instance, a system well known from animal studies to be subject to such programming is the hypothalamic-pituitary-adrenocortical (HPA) axis [23], which is responsible for the regulation of homeostasis and reactions to stress [24], [25]. Antenatal maternal hormones could also disturb development of neuronal processes taking place during gestation. Subtle aberrations in neuronal proliferation, differentiation and migration processes taking place between 6 and 24 weeks of pregnancy, have been suggested to play a role in disorders such as ADHD, autism and some forms of schizophrenia (see [26], [27], [28]).
The present study represents the third wave of the prospective study of Van den Bergh and Marcoen [14] that investigates the influence of antenatal maternal anxiety on different aspects of neurobehavioral development and functioning of their firstborn children. As described above, the long term effects described in the literature by now are regulation problems at cognitive, behavioral and emotional level during childhood. Evidence for these regulation problems was based on mother and/or teacher report; some studies also rely on behavioral observations. The present study is the first one that examines effects of antenatal maternal anxiety into adolescence and the first one in which cognitive functioning (or cognitive regulation problems) is measured with standardized tasks. To this end, two computerized cognitive tasks and two subtests of the Wechsler Intelligence Scale for Children—Revised (WISC-R; [29], [30]) were used.
Through clinical and neurophysiologic studies it is well established that regulation problems and the associated affected functions are critically mediated by the prefrontal cortex in syndromes such as frontal lobe lobectomy, visual neglect and schizophrenia [31], [32], [33] and in at least one subtype of children with ADHD ([34]; see [35] for a review). Consequently, the aim was to investigate the relationship between antenatal maternal anxiety and cognitive tasks, placing a load on prefrontal cortical functions. Three functions were chosen whose link with the prefrontal cortex is well established, namely visual attention control, working memory and response control [33], [36], [37], [38], [39] and these were measured with two cognitive tasks.
Visual attention control is required when subjects have to direct attention to a larger visual area or focus attention to a particular spatial location while ignoring information at other locations. Control of visual attention is mediated by a distributed functional network of areas in frontal and parietal lobes. The frontal areas involved are the medial prefrontal cortex (more specifically anterior cingulate gyrus) [33], and the cluster of areas generally referred to as the frontal eye fields [40], [41]. Working memory load is manipulated by increasing the number of task related elements that have to be maintained at the same time in memory during performance. This function has been associated with the dorsolateral prefrontal cortex [42], [43]. We evaluated visual attention control and working memory with the subtest Encoding of the Amsterdam Neuropsychological Tasks (ANT) [44].
Response control refers to the processes involved in the decision to actually perform a prepared response or to refrain from executing the response. In the present study, response control was assessed with the Stop task paradigm [45], [46], which has been used to monitor the development of inhibitory control [47] and to measure response inhibition in children with disorders such as ADHD, conduct disorder, or anxiety disorders (for a review see [46]). Magnetic resonance imaging (MRI) and functional MRI (fMRI) studies of patients with ADHD have shown abnormalities in fronto-striatal circuitry during performance of stop tasks (e.g. [48], [49]) and other kind or response inhibition tasks (e.g. [50]).
Section snippets
Participants
Of the 86 women and their firstborn children participating at the beginning of the study, 68 participated when the children were 14/15 years old. Of the latter, four adolescents did not participate in the cognitive tasks, data from one outlier were excluded, and data of six other participants could not be used due to computer failure. Consequently, data on 57 mother–child pairs were available for the present study. Twenty-nine of the participants were boys, 28 were girls. The mean age of the
Descriptives and correlational analyses for prenatal State anxiety measures
The mean State anxiety scores for the total group differed depending on the pregnancy period (see Table 1 for descriptive statistics). State12–22 was higher than State23–31(t=3.9, p<0.001) and State32–40(t=2.09; p=0.042). State23–31 and State32–40 did not differ (t=−1.47; p=0.148). As described above, subjects were classified into a high and a low-to-average maternal anxiety group for each pregnancy period, with Pc75 as cut-off score. The values of Pc75 are similar (for State12–22) or slightly
Discussion
This study prospectively investigated the influence of maternal State anxiety measured at 12–22, 23–31 and 32–40 weeks of pregnancy, on cognitive functioning in adolescents. ANCOVAs showed an effect of anxiety at 12–22 weeks only. Adolescents of mothers who were highly anxious during the 12–22nd week of pregnancy responded faster in the Encoding task and made more errors in the target present condition of that task, indicating an impulsive response pattern. They also scored significantly lower
References (70)
The role of prenatal stress in the etiology of developmental behavioural disorders
Neurosci Biobehav Rev
(2002)- et al.
Prenatal maternal stress: effects on pregnancy and the (unborn) child
Early Hum Dev
(2002) - et al.
Maternal anxiety in late pregnancy: effect on fetal movements and fetal heart rate
Early Hum Dev
(2002) - et al.
The effect of (induced) maternal emotions on fetal behaviour: a controlled study
Early Hum Dev
(1989) Issues in the diagnosis of attention-deficit/hyperactivity disorder in children
Brain Dev
(2003)The dynamic approach to neurodevelopmental psychiatric disorders: use of fMRI combined with neuropsychology to elucidate the dynamics of psychiatric disorders, exemplified in ADHD and schizophrenia
Behav Brain Res
(2002)Trajectories of brain development: point of vulnerability or window of opportunity?
Neurosci Biobehav Rev
(2003)- et al.
Neurotransmitters and neuromodulators during early human development
Early Hum Dev
(2001) Endocrine programming and fetal origins of adult disease
Trends Endocrinol Metab
(2002)- et al.
Drug exposure early in life: functional repercussions of changing neuropharmacology during sensitive periods of brain development
Curr Opin Pharmacol
(2004)
Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitatary-adrenocortical responsiveness
Front Neuroendocrinol
The neurobiology of stress: from serendipity to clinical relevance
Brain Res
Differential frontal activation in schizophrenia and bipolar illness during verbal fluency
J Affect Disord
Biological contributions to the presentation and understanding of attention-deficit/hyperactivity disorder: a review
Clin Psychol Rev
Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: a tutorial review
Conscious Cogn
The prefrontal cortex–an update: time is of the essence
Neuron
Contributions of the prefrontal cortex to the neural basis of human decision making
Neurosci Biobehav Rev
A common network of functional areas for attention and eye movements
Neuron
Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network
Neuroimage
Response inhibition and response re-engagement in attention-deficit/hyperactivity disorder, disruptive, anxious and normal children
Behav Brain Res
Differential patterns of striatal activtion in young children with and without ADHD
Biol Psychiatry
Information processing characteristics in subtypes of multiple sclerosis
Neuropsychologia
Ontogenesis of goal-directed behavior: anatomo-functional considerations
Int J Psychophysiol
Emotion in the perspective of an integrated nervous system
Brain Res Rev
The prefrontal cortex: complex neural properties for complex behavior
Neuron
Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?
Psychol Bull
Antenatal maternal anxiety and stress and the neurobehavioral development of fetus and child: links and possible mechanisms. A review
Neurosci Biobehav Rev
Maternal stress and affect influence fetal neurobehavioral development
Dev Psychol
Maternal anxiety during pregnancy: effect on fetal behavior at 38 to 40 weeks of gestation
J Dev Behav Psychiatry
The influence of maternal emotions during pregnancy on fetal and neonatal behavior
Pre Perinat Psychol J
Epidemiological studies of stress during pregnancy and fetal brain development. Doctoral dissertation
Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years: report from the Avon Longitudinal Study of Parents and Children
Br J Psychiatry
Maternal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis
J Child Psychol Psychiatry
Are maternal smoking and stress during pregnancy related to ADHD symptoms in children?
J Child Psychol Psychiatry
High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems and anxiety in 8/9-Year-Olds
Child Dev
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