The developmental cognitive neuroscience of functional connectivity

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Abstract

Developmental cognitive neuroscience is a rapidly growing field that examines the relationships between biological development and cognitive ability. In the past decade, there has been ongoing refinement of concepts and methodology related to the study of ‘functional connectivity’ among distributed brain regions believed to underlie cognition and behavioral control. Due to the recent availability of relatively easy-to-use tools for functional connectivity analysis, there has been a sharp upsurge of studies that seek to characterize normal and psychopathologically abnormal brain functional integration. However, relatively few studies have applied functional and effective connectivity analysis techniques to developmental cognitive neuroscience. Functional and effective connectivity analysis methods are ideally suited to advance our understanding of the neural substrates of cognitive development, particularly in understanding how and why changes in the functional ‘wiring’ of neural networks promotes optimal cognitive control throughout development. The purpose of this review is to summarize the central concepts, methods, and findings of functional integration neuroimaging research to discuss key questions in the field of developmental cognitive neuroscience. These ideas will be presented within a context that merges relevant concepts and proposals from different developmental theorists. The review will outline a few general predictions about likely relationships between typical ‘executive’ cognitive maturation and changes in brain network functional integration during adolescence. Although not exhaustive, this conceptual review also will showcase some of recent findings that have emerged to support these predictions.

Section snippets

Organization of review

Developmental cognitive neuroscience is a rapidly growing field that examines the relationships between biological development and cognitive ability. Although the field is derived most directly from theoretical models of cognitive development informed by biological studies of brain maturation, it also draws upon many concepts taken from psychology, neuroscience, social science, and genetics in an effort to better describe specific mechanisms that influence developmental changes in cognition.

The limitations of functional specialization

As a result of the widespread use of functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and electrophysiological recordings (EEG) over the past several decades, there is now a considerable scientific literature to draw upon for understanding the neural basis of cognitive development (see recent reviews by Casey et al., 2005, Casey and Munakata, 2002, Diamond and Amso, 2008, Durston and Casey, 2006, Durston et al., 2006, Johnson, 2001, Johnson, 2005, Kuhn, 2006,

Functional integration informs theories of neural organization and development

In this section, we will discuss how the concepts reviewed above can inform theories of brain function, neural organization, and cognitive development. Given the premise that ‘functional integration’ refers generally to the degree to which widely-distributed brain regions are engaged in a coordinated manner or influence each other in meaningful ways, one might ask, “So, why do brain regions become functionally integrated?” It has been suggested that functional integration represents a

Basic predictions for executive functional neural network development

The inclusion of the concept of functional integration to neural constructivist models has led to a number of theoretical predictions about executive cognitive development. This section will outline some of these predictions and describe recent empirical support for each.

Review summary and future directions

The purpose of the current review was to highlight the potential to more greatly understand cognitive development through use of functional integration analysis methods. This review is admittedly selective in its focus on both fMRI research and neural constructivism because the majority of recent empirical reports utilize these concepts and methods. It also necessarily omitted many of the significant conceptual contributions made from PET and EEG research in order to retain its primary focus.

Conclusions

This review has provided a theoretical and empirical overview of the study of neuronal functional integration in developmental cognitive neuroscience. As this field continues to evolve, the upsurge of interest in using recently developed functional neuroimaging analysis techniques will no doubt spark numerous new lines of inquiry relevant to cognitive development. The current review argues that by including functional integration concepts into existing theories of neural development, reasonable

References (160)

  • B.J. Casey et al.

    Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder

    Journal of the American Academy of Child & Adolescent Psychiatry

    (1997)
  • B.J. Casey et al.

    Changes in cerebral functional organization during cognitive development

    Current Opinion Neurobiology

    (2005)
  • F. Collette et al.

    Exploration of the neural substrates of executive functioning by functional neuroimaging

    Neuroscience

    (2006)
  • D. Cordes et al.

    Hierarchical clustering to measure connectivity in fMRI resting-state data

    Magnetic Resonance Imaging

    (2002)
  • J. Daunizeau et al.

    Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework

    Neuroimage

    (2007)
  • O. David et al.

    Modelling event-related responses in the brain

    Neuroimage

    (2005)
  • M.C. Davidson et al.

    Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching

    Neuropsychologia

    (2006)
  • N.U. Dosenbach et al.

    A dual-networks architecture of top–down control

    Trends in Cognitive Sciences

    (2008)
  • J. Duncan et al.

    Common regions of the human frontal lobe recruited by diverse cognitive demands

    Trends in Neurosciences

    (2000)
  • S. Durston et al.

    What have we learned about cognitive development from neuroimaging?

    Neuropsychologia

    (2006)
  • A.A. Fingelkurts et al.

    Functional connectivity in the brain -- Is it an elusive concept?

    Neuroscience and Biobehavioral Reviews

    (2005)
  • P. Fries

    A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence

    Trends in Cognitive Sciences

    (2005)
  • K.J. Friston et al.

    Dynamic causal modelling

    Neuroimage

    (2003)
  • J.M. Fuster

    The cognit: A network model of cortical representation

    International Journal of Psychophysiology

    (2006)
  • W.D. Gaillard et al.

    Developmental aspects of pediatric fMRI: Considerations for image acquisition, analysis, and interpretation

    Neuroimage

    (2001)
  • L.M. Harrison et al.

    Extra-classical receptive field effects measured in striate cortex with fMRI

    Neuroimage

    (2007)
  • B. Horwitz

    The elusive concept of brain connectivity

    Neuroimage

    (2003)
  • M. Huizinga et al.

    Age-related change in executive function: Developmental trends and a latent variable analysis

    Neuropsychologia

    (2006)
  • A.A. Ioannides

    Dynamic functional connectivity

    Current Opinion Neurobiology

    (2007)
  • D.P. Kennedy et al.

    The intrinsic functional organization of the brain is altered in autism

    Neuroimage

    (2008)
  • T. Klingberg

    Development of a superior frontal-intraparietal network for visuo-spatial working memory

    Neuropsychologia

    (2006)
  • T. Koenig et al.

    Millisecond by millisecond, year by year: Normative EEG microstates and developmental stages

    Neuroimage

    (2002)
  • B. Kolb

    Overview of cortical plasticity and recovery from brain injury

    Physical Medicine and Rehabilitation Clinics of North America

    (2003)
  • B. Luna et al.

    Maturation of widely distributed brain function subserves cognitive development

    Neuroimage

    (2001)
  • E. Macaluso et al.

    Multisensory spatial interactions: A window onto functional integration in the human brain

    Trends in Neurosciences

    (2005)
  • V.A. Makarov et al.

    A method for determining neural connectivity and inferring the underlying network dynamics using extracellular spike recordings

    Journal of Neuroscience Methods

    (2005)
  • G. Marrelec et al.

    Regions, systems, and the brain: Hierarchical measures of functional integration in fMRI

    Medical Image Analysis

    (2008)
  • V. Menon et al.

    Maturation of medial temporal lobe response and connectivity during memory encoding

    Brain Research Cognitive Brain Research

    (2005)
  • S. Achard et al.

    A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs

    The Journal of Neuroscience

    (2006)
  • P. Anderson

    Assessment and development of executive function (EF) during childhood

    Child Neuropsychology

    (2002)
  • V.A. Anderson et al.

    Development of executive functions through late childhood and adolescence in an Australian sample

    Developmental Neuropsychology

    (2001)
  • C. Babiloni et al.

    Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis

    Behavioral Neuroscience

    (2004)
  • E.H. Baeg et al.

    Learning-induced enduring changes in functional connectivity among prefrontal cortical neurons

    The Journal of Neuroscience

    (2007)
  • A.A. Baird et al.

    Functional connectivity: Integrating behavioral, diffusion tensor imaging, and functional magnetic resonance imaging data sets

    Journal of Cognitive Neuroscience

    (2005)
  • D. Balduzzi et al.

    Integrated information in discrete dynamical systems: Motivation and theoretical framework

    PLoS Computational Biology

    (2008)
  • D.S. Barth

    Submillisecond synchronization of fast electrical oscillations in neocortex

    The Journal of Neuroscience

    (2003)
  • C.F. Beckmann et al.

    Investigations into resting-state connectivity using independent component analysis

    Philosophical Transactions of the Royal Society of London B Biological Sciences

    (2005)
  • L. Biagi et al.

    Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling

    Journal of Magnetic Resonance Imaging

    (2007)
  • T. Bitan et al.

    The interaction between orthographic and phonological information in children: An fMRI study

    Human Brain Mapping

    (2007)
  • S.J. Blakemore et al.

    Development of the adolescent brain: Implications for executive function and social cognition

    Journal of Child Psychology and Psychiatry and Allied Disciplines

    (2006)
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