Elsevier

Neuropsychologia

Volume 48, Issue 12, October 2010, Pages 3573-3579
Neuropsychologia

Top-down control of MEG alpha-band activity in children performing Categorical N-Back Task

https://doi.org/10.1016/j.neuropsychologia.2010.08.006Get rights and content

Abstract

Top-down cognitive control has been associated in adults with the prefrontal–parietal network. In children the brain mechanisms of top-down control have rarely been studied. We examined developmental differences in top-down cognitive control by monitoring event-related desynchronization (ERD) and event-related synchronization (ERS) of alpha-band oscillatory activity (8–13 Hz) during anticipation, target detection and post-response stages of a visual working memory task. Magnetoencephalography (MEG) was used to record brain oscillatory activity from healthy 10-year-old children and young adults performing the Categorical N-Back Task (CNBT). Neuropsychological measures assessing frontal lobe networks were also acquired. Whereas adults showed a modulation of the ERD at the anticipatory stages of CNBT and ERS at the post-response stage, children displayed only some anticipatory modulation of ERD but no ERS at the post-response stage, with alpha-band remaining at a desynchronized state. Since neuropsychological and prior neuroimaging findings indicate that the prefrontal–parietal networks are not fully developed in 10-year olds, and since the children performed as well as the adults on CNBT and yet displayed different patterns of ERD/ERS, we suggest that children may be using different top-down cognitive strategies and, hence, different, developmentally apt neuronal networks.

Research highlights

▶ The prefrontal–parietal networks associated with top-down cognitive control in adults are not matured in 10-year olds, yet children perform well on visual-working memory tasks. ▶ We use magnetoencephalography (MEG) to monitor in children and adults event-related desynchronization (ERD) and synchronization (ERS) of parietal–occipital alpha-band oscillatory activity (8–13 Hz) during top-down anticipatory, target detection and post-response stages of the Categorical N-Back Task (CNBT). ▶ Since children performed as well as the adults on CNBT and yet displayed developmentally distinct, task-stage-determined patterns of ERD/ERS we suggest that children may be using different top-down cognitive strategies and, hence, different, developmentally apt neuronal networks.

Introduction

Top-down cognitive control is driven by a set of task-related rules. Commonly, it refers to the influence of information stored at higher neuronal centers upon sensory perceptual and motor networks, and serves the selection of target stimuli and responses. Top-down control is overtly revealed in brain activation related to anticipation of a target. Such anticipatory activation may engage task-specific networks related to spatial localization, object categorization, or maintenance of working memory (Martin et al., 2000, Mishkin et al., 1983, Rizzolatti and Matelli, 2003, Serences et al., 2004, Worden et al., 2000). The neural network that has been associated with visual top-down control encompasses lateral (dorsal frontal, inferior parietal) and medial (cingulate, temporal–occipital) cortical regions (Buckner and Carroll, 2007, Corbetta and Shulman, 2002, Raichle et al., 2001, Serences and Yantis, 2006, Shulman et al., 1997). Mental chronometry studies have suggested varying degrees of frontal–parietal engagement at different stages of cognitive tasks (Halgren et al., 2002, Posner and Rueda, 2002, Sternberg, 1969). To our knowledge, neuroimaging data on the chronometry of top-down anticipatory processing in children has not been reported. Here we investigate the developmental differences in parietal–occipital activity related to top-down attentional control employed during consecutive stages of a visual working memory task.

The visual working memory task we used, Categorical N-Back Task (CNBT) (Ciesielski, Lesnik, Savoy, Grant, & Ahlfors, 2006), is a new variant of the classical n-back working-memory task (Gevins & Cutillo, 1993). It was designed (by KTC) as a computer game for children (Ciesielski, Lesnik, Ahlfors, Savoy, & Baedorf, 2004). As a working memory paradigm it refers to time-limited processes of active memory representation of knowledge that is accessible later for further manipulation (Baddeley, 1986). Thus, CNBT is a complex object-working memory paradigm, well suited for dissection of cognitive stages comprising stringent attentional focusing, active memory encoding, anticipation of a target according to internalized rules, cognitive categorical judgment and motor response. CNBT maximizes demands for executive reasoning, while holding memory demands constant. Effective manipulation of mental representations, actively held “on line”, while inhibiting irrelevant events has been found to be a valid indicator of mental flexibility and cognitive development (Gevins and Smith, 2000, Johnson et al., 2001). During CNBT the subject was required to respond to the target (raccoon) when at least two stimuli prior to the target belonged to a designated category of animals. Presentation of multiple consecutive pictures of animals served as a prompt, gradually increasing the subject's anticipation and, therefore, the attentional readiness for target detection and response. Thus, CNBT is a temporal cueing paradigm in which allocation of attentional resources can be monitored during its chronometric stages: anticipatory (two-back and one-back before target, 2BT, 1BT), target detection (T), and post-response (PR). Correct performance on CNBT relies on effective top-down management of preparatory cues and control of response to targets.

We used magnetoencephalography (MEG) to examine developmental differences in top-down attentional control reflected in the modulation of alpha-band (8–13 Hz) activity at different stages of CNBT. Alpha-band activity has been found to be a sensitive indicator of cognitive task demands (Gevins et al., 1979, Gevins et al., 1997, Lisman and Idiart, 1995, Nunez et al., 2001). Early studies showed a systematic reduction of alpha in tasks with increasing memory loads (Gevins et al., 1979). Reduction of alpha, subsequent to extrinsic or intrinsic events was termed event-related desynchronization (ERD), whereas an increase in alpha was termed event-related synchronization (ERS) (Pfurtscheller & Aranibar, 1977). It has been suggested that the modulation of alpha-band activity reveals the cognitive strategies used by individual subjects during effortful anticipatory processing and represents a voluntary inhibitory activation of task irrelevant networks (Foxe et al., 1998, Gevins and Cutillo, 1993, Smith and Jonides, 1999, Worden et al., 2000).

Electrophysiological and neuroimaging evidence on the developmental trajectory in top-down attentional processing is scant. Evidence suggests that the facility for top-down attentional modulation at early stages of sensory processing continues to change during childhood and early adolescence (Bunge et al., 2002, Poggel and Strasburger, 2004, Taylor et al., 2003), and that those developmental changes show task and stimulus specific characteristics (Greenaway & Plaisted, 2005). Similar findings have been reported in studies on top-down attentional control in children, as reflected in oscillatory activity (Klimesch et al., 2001, Krause et al., 2001). Studies in adults have focused on spatial cortical distribution and increased coherence of alpha and theta (3–7 Hz) activity during attentional tasks (Babiloni et al., 2005a, Gevins and Smith, 2000). Thalamo-cortical and cortical–cortical networks involving the parietal–occipital cortex have been associated with alpha generators (Hari and Salmelin, 1997, Pfurtscheller, 1992, Schnitzler and Gross, 2005, Steriade and Llinas, 1988). In the present study we examined child–adult differences in performance and in modulation of parietal activity within the alpha-band during consecutive stages of the object-working memory task, the CNBT.

Our earlier fMRI studies with CNBT demonstrated an intriguing dissociation in children between high, adult-like performance accuracy and reduced task-related engagement of the ventral prefrontal networks, predominant in adults. In contrast to adults, children displayed activation within a developmentally determined network of posterior parietal, premotor and subcortical brain regions (Ciesielski et al., 2006). Based on these earlier findings, and on the fact that parietal-occipital alpha has been reported to be immature in 10–12 year olds (Krause et al., 2001, Krause et al., 2007), we expected in the present study that the performance in children may be similar to adults, but their pattern of MEG alpha activation may vary.

The outcome of top-down cognitive strategies that we measure here in patterns of alpha activation within different stages of CNBT is determined by maturation of distributed brain networks, including the frontal–parietal. Since frontal components of these networks are not fully developed until late adolescence (Atkinson et al., 2006, Bunge et al., 2002, Gogtay et al., 2006, Huttenlocher, 1990), we hypothesized that the ERD/ERS pattern of top-down alpha modulation in children is different from that in adults. Considering that the trajectory of cognitive development progresses from sensory-motor to internalized ability to predict (Piaget, 1971, Luciana and Nelson, 1998), we expected the most prominent differences in alpha activation between children and adults at the anticipatory task stages.

Section snippets

Participants

Twelve healthy right-handed volunteers participated in the study: six 10-year-old children (9y3mo–10y5mo; mean 9y9mo; 3 males/3 females) and six young adults (20y3mo–27y8mo, mean 23.9; 3 males/3 females). We used rigorous criteria to select healthy children and adults. All subjects participated in a neuropsychological session several weeks prior to the MEG testing. Psychometric IQ in WAIS and WISC testing (children mean: 118, +/−9; adults: 120, +/−11) were complemented by neuropsychological

Behavior

No significant differences between the children and adults were found in the performance on the CNBT (Table 1A). The mean response accuracy was high in both groups (children: 90.7%; adults: 94.7%) ranging in individual subjects and ranging in indvidual subjects between 86% and 96%, which corresponds to 36–39 correct trials from 42 available. The mean RTs were 436 ms for children and 401 ms for adults.

Table 1B displays results of neuropsychological tests. No significant differences between

Discussion

We examined top-down attentional modulation of alpha-band oscillatory activity related to three different stages of the visual working memory task, the CNBT, in 10-year-old children and young adults: the anticipatory stage, target detection, and post-response. Although the sensory, bottom-up information was identical in both children and adults, the pattern of top-down event-related alpha modulation was different. In adults, the proximity of the anticipatory stimuli to the forthcoming target

Acknowledgements

We thank Drs Bruce Rosen for his continuous support and Mark Vangel for helpful comments. Study was supported in part by the National Center for Research Resources (P41RR14075). Authorship: KTC and MSH are both senior authors.

References (71)

  • W. Klimesch et al.

    Simultaneous desynchronization and synchronization of different alpha responses in the human electroencephalograph: A neglected paradox?

    Neuroscience Letters

    (2000)
  • W. Klimesch et al.

    Alpha and beta band power changes in normal and dyslexic children

    Clinical Neurophysiology

    (2001)
  • C.M. Krause et al.

    Event-related desynchronization and synchronization during a memory task in children

    Clinical Neurophysiology

    (2001)
  • M. Luciana et al.

    The functional emergence of prefrontally-guided working memory systems in four- to eight-year-old children

    Neuropsychologia

    (1998)
  • M. Mishkin et al.

    Object vision and spatial vision: Two cortical pathways

    Trends in Neurosciences

    (1983)
  • D.A. Norman et al.

    On data-limited and resource-limited processes

    Cognitive Psycholology

    (1975)
  • G. Pfurtscheller et al.

    Event-related cortical desynchronization detected by power measurements of scalp EEG

    Electroencephalography and Clinical Neurophysiology

    (1977)
  • G. Pfurtscheller

    Event-related synchronization (ERS): An electrophysiological correlate of cortical areas at rest

    Electroencephalography and Clinical Neurophysiology

    (1992)
  • R. Salmelin et al.

    Characterization of spontaneous MEG rhythms in healthy adults

    Electroencephalography and Clinical Neurophysiology

    (1994)
  • J.D. Schmahmann et al.

    The cerebrocerebellar system

  • J.T. Serences et al.

    Selective visual attention and perceptual coherence

    Trends in Cognitive Science

    (2006)
  • M.J. Taylor et al.

    Discrimination of single features and conjunctions by children

    International Journal of Psychophysiology

    (2003)
  • C. Babiloni et al.

    Human alpha rhythms during visual delayed choice reaction time tasks: A magnetoencephalography study

    Human Brain Mapping

    (2005)
  • C. Babiloni et al.

    Pre- and poststimulus alpha rhythms are related to conscious visual perception: A high-resolution EEG study

    Cerebral Cortex

    (2006)
  • A. Baddeley

    Working memory

    (1986)
  • S.L. Bressler et al.

    Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention

    Journal of Neuroscience

    (2008)
  • D.E. Broadbent

    Perception and communication

    (1958)
  • C. Buchel et al.

    Modulation of connectivity in visual pathways by attention: Cortical interactions evaluated with structural equation modelling and fMRI

    Cerebral Cortex

    (1997)
  • R.L. Buckner et al.

    The brain's default network: Anatomy, function, and relevance to disease

    Annals of the New York Academy of Sciences

    (2008)
  • G. Buzsáki

    Rhythms of the brain

    (2006)
  • K.T. Ciesielski et al.

    Developmental pattern of activation within the prefrontal–cerebellar subsystem in a new Categorical N-Back Task

  • K.T. Ciesielski et al.

    MRI morphometry of mamillary bodies, caudate nuclei, and prefrontal cortices after chemotherapy for childhood leukemia: Multivariate models of early and late developing memory subsystems

    Behavioral Neuroscience

    (1999)
  • D.M. Clower et al.

    Basal ganglia and cerebellar inputs to ‘AIP’

    Cerebral Cortex

    (2005)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nature Review Neuroscience

    (2002)
  • R. Desimone et al.

    Neural mechanisms of selective visual attention

    Annual Review of Neuroscience

    (1995)
  • Cited by (0)

    View full text