Elsevier

NeuroImage

Volume 30, Issue 3, 15 April 2006, Pages 679-691
NeuroImage

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Functional imaging of developmental and adaptive changes in neurocognition

https://doi.org/10.1016/j.neuroimage.2005.10.007Get rights and content

Abstract

Characterization of brain–behavior relationships through functional magnetic imaging (fMRI) within typically or atypically developing populations poses methodological and interpretational challenges. We consider theoretical, methodological, and artifactual factors that influence characterization of developmental and adaptive changes in childhood. Findings from anatomical and physiological brain development studies are highlighted as they may influence functional imaging results. Then, we consider several patterns of functional activation within the context of developmental processes as well as neurologic disease. Hypotheses regarding the development of cognitive networks are proposed to account for the individual differences seen in normal and atypical development. We also identify potential sources of unwanted variability related to experimental design and task performance and suggest possible solutions to help minimize these effects. Lastly, a challenge for current studies is a lack of group and individual analysis methods that can be reliably applied to capture and quantify factors that contribute to variability introduced by developmental and disease processes. We review current methods and propose potential solutions.

Introduction

Functional magnetic resonance imaging (fMRI) has permitted characterization of brain–behavior relationships with increasing precision. Characterization of those relationships within typically or atypically developing populations, however, poses methodological and interpretational challenges that differ from those pertinent to adult populations. Specifically, two factors distinguish investigation of child and adult neurocognition. First, characterization of the neural basis of cognition in children must be made against the backdrop of ongoing biological maturation. With variable rates of biological maturation, children of the same age are likely to differ more than adults of the same age. Thus, individual variability must be characterized more fully in investigation of developing rather than mature cognition. Second, adaptive changes following developmental or acquired disorders may differ in structural and functional characteristics relative to those following adult neurologic injury. As an end state of maturation, adulthood represents completed functional organization. Functional recovery following adult neurological injury, therefore, must be accomplished by compensatory processing enabled by neural reorganization. In contrast, as a state of ongoing maturation, childhood represents incomplete functional organization. Childhood disorders, therefore, alter the course of functional organization. Functional outcomes are likely to differ following adaptive changes in childhood relative to adulthood. Thus, models of functional organization gleaned from adult studies are limited in revealing adaptive changes in neurocognition. Taken together, these factors result in neurocognitive adaptive changes in children that are unlikely to be homogeneous because biological and experiential factors interact in a variety of ways. Consequently, there may be multiple variants of typical and atypical development.

This paper will consider theoretical, methodological, and artifactual factors that influence characterization of developmental and adaptive changes in childhood. Current functional neuroimaging methods are optimized for elucidating invariant properties of cognition as embodied in adulthood, and therefore, are limited in revealing a complete picture of developmental and adaptive variability in brain–behavior relationships. While others have considered some of these factors, the present discussion will focus on these issues as they pertain specifically to the investigation of developing populations.

Section snippets

Neuroanatomic and physiological changes

A detailed review of anatomical and physiological brain development is not undertaken in this paper; however, the following summary of findings provides the context in which developmental functional imaging studies are interpreted. The structural and physiological changes taking place in a developing brain may influence functional imaging data. In addition to normal brain maturation, pediatric disease processes may further affect functional imaging data. Key findings are summarized and then the

Classification of patterns of functional activation

In this section, we consider several patterns of functional activation within the context of developmental processes as well as neurologic disease. Hypotheses regarding the development of cognitive networks are proposed to account for the individual differences seen in normal and atypical development. A fundamental goal of developmental studies that use fMRI is to identify the normal neural network that underlies a cognitive process as reflected by task specific activation (Fig. 2). However,

Variability sources and solutions

Sources of variability may be introduced at many points during experimentation including decisions regarding experimental design, image acquisition, and processing. As measurement and data processing factors such as motion artifact (Gaillard et al., 2003c), equipment issues (e.g., head coil for pediatric patients) (Gaillard et al., 2001a, Henry et al., 2001, Lipschutz et al., 2001), scanning preparation (Byars et al., 2002, Slifer, 1996, Slifer et al., 1994, Slifer et al., 2002), and a

Assessing variability

A challenge for current studies is a lack of group and individual analysis methods that can be reliably applied to capture and quantify factors that contribute to variability introduced by developmental and disease processes. An assumption of group comparison studies is that the individual groups are homogeneous; however, this assumption is misleading, particularly with diseased and developmentally disabled populations. As proposed earlier, there are a number of potential normal variants

Conclusions

Characterization of the functional anatomy of developmental and adaptive neurocognitive changes poses unique challenges. Models of functional organization gleaned from adults are limited in revealing developmental and adaptive changes because they underestimate variability among individuals. Individual differences are enhanced during typical and atypical development as a result of interactive effects of maturational and experiential factors. Guided by findings of extant studies, we have

Acknowledgments

Supported by NINDS RO1 NS44280, NIMH RO1 MH65395; Mental Retardation and Developmental Disabilities Core NICHD P30HD40677, Children's National Medical Center, and Clinical Epilepsy Section, NINDS, NIH.

References (122)

  • W.D. Gaillard et al.

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

    NeuroImage

    (2001)
  • S.K. Holland et al.

    Normal fMRI brain activation patterns in children performing a verb generation task

    NeuroImage

    (2001)
  • B. Horwitz

    The elusive concept of brain connectivity

    NeuroImage

    (2003)
  • H.C. Kang et al.

    Comparison of functional activation foci in children and adults using a common stereotactic space

    NeuroImage

    (2003)
  • L. Lee et al.

    A report of the functional connectivity workshop, Dusseldorf 2002

    NeuroImage

    (2003)
  • B. Lipschutz et al.

    Assessing study-specific regional variations in fMRI signal

    NeuroImage

    (2001)
  • R.S. Liu et al.

    A longitudinal quantitative MRI study of community-based patients with chronic epilepsy and newly diagnosed seizures: methodology and preliminary findings

    NeuroImage

    (2001)
  • B. Luna et al.

    Maturation of widely distributed brain function subserves cognitive development

    NeuroImage

    (2001)
  • A.R. McIntosh et al.

    Spatial pattern analysis of functional brain images using partial least squares

    Neuroimage

    (1996)
  • O. Muzik et al.

    Statistical parametric mapping: assessment of application in children

    NeuroImage

    (2000)
  • R.A. Poldrack

    Imaging brain plasticity: conceptual and methodological issues—A theoretical review

    NeuroImage

    (2000)
  • K. Rubia et al.

    Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI

    Neurosci. Biobehav. Rev.

    (2000)
  • S. Saxena et al.

    Functional neuroimaging and the neuroanatomy of obsessive–compulsive disorder

    Psychiatry Clin. North Am.

    (2000)
  • B.A. Shaywitz et al.

    Disruption of posterior brain systems for reading in children with developmental dyslexia

    Biol. Psychiatry

    (2002)
  • S.E. Shaywitz et al.

    Neural systems for compensation and persistence: young adult outcome of childhood reading disability

    Biol. Psychiatry

    (2003)
  • K.J. Slifer

    A video system to help children cooperate with motion control for radiation treatment without sedation

    J. Pediatr. Oncol. Nurs.

    (1996)
  • Z. Ahmad et al.

    Auditory comprehension of language in young children: neural networks identified with fMRI

    Neurology

    (2003)
  • W.H. Backes et al.

    Atypical brain activation of reading processes in children with developmental dyslexia

    J. Child Neurol.

    (2002)
  • Ball, Jr., W.S., Holland, S.K., 2001. Perfusion imaging in the pediatric patient. Magn. Reson. Imaging Clin. N. Am., 9...
  • L. Balsamo

    Neural representation and function of language in children with new onset partial epilepsy

  • L.M. Balsamo et al.

    A functional magnetic resonance imaging study of left hemisphere language dominance in children

    Arch. Neurol.

    (2002)
  • I. Baron

    Neuropsychological Evaluation of the Child

    (2004)
  • J.R. Binder et al.

    Determination of language dominance using functional MRI: a comparison with the wada test

    Neurology

    (1996)
  • J.R. Binder et al.

    Human temporal lobe activation by speech and nonspeech sounds

    Cereb. Cortex Mon.

    (2000)
  • S.Y. Bookheimer

    Methodological issues in pediatric neuroimaging

    Ment. Retard. Dev. Disabil. Res. Rev.

    (2000)
  • S. Bookheimer et al.

    Regional cerebral blood flow during object naming and word reading

    Hum. Brain Mapp.

    (1995)
  • J.R. Booth et al.

    Developmental and lesion effects in brain activation during sentence comprehension and mental rotation

    Dev. Neuropsychol.

    (2000)
  • J.R. Booth et al.

    The development of specialized brain systems in reading and oral-language

    Neuropsychol. Dev. Cogn., Sect. C, Child Neuropsychol.

    (2001)
  • J.P. Bourgeois et al.

    Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction

    Proc. Natl. Acad. Sci. U. S. A.

    (1989)
  • J.P. Bourgeois et al.

    Synaptogenesis in the prefrontal cortex of rhesus monkeys

    Cereb. Cortex

    (1994)
  • T.T. Brown et al.

    Developmental changes in human cerebral functional organization for word generation

    Cereb. Cortex

    (2005)
  • A.W. Byars et al.

    Practical aspects of conducting large-scale functional magnetic resonance imaging studies in children

    J. Child Neurol.

    (2002)
  • B.J. Casey et al.

    A developmental functional MRI study of prefrontal activation during performance of a go–no-go task

    J. Cogn. Neurosci.

    (1997)
  • B.J. Casey et al.

    Dissociating striatal and hippocampus function developmentally with a stimulus–response compatibility task

    J. Neurosci.

    (2002)
  • F.X. Castellanos et al.

    Quantitative morphology of the caudate nucleus in attention deficit hyperactivity disorder

    Am. J. Psychiatry

    (1994)
  • F.X. Castellanos et al.

    Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder

    JAMA

    (2002)
  • V.S. Caviness et al.

    The human brain age 7–11 years: a volumetric analysis based on magnetic resonance images

    Cereb. Cortex

    (1996)
  • C. Chiron et al.

    Changes in regional cerebral blood flow during brain maturation in children and adolescents

    J. Nucl. Med.

    (1992)
  • H.T. Chugani et al.

    The lennox-gastaut syndrome: metabolic subtypes determined by 2-deoxy-2[18f]fluoro-d-glucose positron emission tomography

    Ann. Neurol.

    (1987)
  • L. Cohen et al.

    The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients

    Brain

    (2000)
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