Comments and ControversiesFunctional imaging of developmental and adaptive changes in neurocognition☆
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)
- et al.
Functional activation patterns in adults, children, and pediatric patients with brain lesions
Prog. Neuro-Psychopharmacol. Biol. Psychiatry
(1999) - et al.
A parametric study of prefrontal cortex involvement in human working memory
NeuroImage
(1997) - et al.
Immature frontal lobe contributions to cognitive control in children: evidence from fMRI
Neuron
(2002) - et al.
The feasibility of a common stereotactic space for children and adults in fMRI studies of development
NeuroImage
(2002) - et al.
Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI
NeuroImage
(1995) - et al.
Changes in cerebral functional organization during cognitive development
Curr. Opin. Neurobiol.
(2005) - et al.
Imaging the developing brain: what have we learned about cognitive development?
Trends Cogn. Sci.
(2005) - et al.
Deformation-based surface morphometry applied to gray matter deformation
NeuroImage
(2003) - et al.
Multisubject fMRI studies and conjunction analyses
NeuroImage
(1999) Functional MR imaging of language, memory, and sensorimotor cortex
Neuroimaging Clin. N. Am.
(2004)
Developmental aspects of pediatric fMRI: considerations for image acquisition, analysis, and interpretation
NeuroImage
Normal fMRI brain activation patterns in children performing a verb generation task
NeuroImage
The elusive concept of brain connectivity
NeuroImage
Comparison of functional activation foci in children and adults using a common stereotactic space
NeuroImage
A report of the functional connectivity workshop, Dusseldorf 2002
NeuroImage
Assessing study-specific regional variations in fMRI signal
NeuroImage
A longitudinal quantitative MRI study of community-based patients with chronic epilepsy and newly diagnosed seizures: methodology and preliminary findings
NeuroImage
Maturation of widely distributed brain function subserves cognitive development
NeuroImage
Spatial pattern analysis of functional brain images using partial least squares
Neuroimage
Statistical parametric mapping: assessment of application in children
NeuroImage
Imaging brain plasticity: conceptual and methodological issues—A theoretical review
NeuroImage
Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI
Neurosci. Biobehav. Rev.
Functional neuroimaging and the neuroanatomy of obsessive–compulsive disorder
Psychiatry Clin. North Am.
Disruption of posterior brain systems for reading in children with developmental dyslexia
Biol. Psychiatry
Neural systems for compensation and persistence: young adult outcome of childhood reading disability
Biol. Psychiatry
A video system to help children cooperate with motion control for radiation treatment without sedation
J. Pediatr. Oncol. Nurs.
Auditory comprehension of language in young children: neural networks identified with fMRI
Neurology
Atypical brain activation of reading processes in children with developmental dyslexia
J. Child Neurol.
Neural representation and function of language in children with new onset partial epilepsy
A functional magnetic resonance imaging study of left hemisphere language dominance in children
Arch. Neurol.
Neuropsychological Evaluation of the Child
Determination of language dominance using functional MRI: a comparison with the wada test
Neurology
Human temporal lobe activation by speech and nonspeech sounds
Cereb. Cortex Mon.
Methodological issues in pediatric neuroimaging
Ment. Retard. Dev. Disabil. Res. Rev.
Regional cerebral blood flow during object naming and word reading
Hum. Brain Mapp.
Developmental and lesion effects in brain activation during sentence comprehension and mental rotation
Dev. Neuropsychol.
The development of specialized brain systems in reading and oral-language
Neuropsychol. Dev. Cogn., Sect. C, Child Neuropsychol.
Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction
Proc. Natl. Acad. Sci. U. S. A.
Synaptogenesis in the prefrontal cortex of rhesus monkeys
Cereb. Cortex
Developmental changes in human cerebral functional organization for word generation
Cereb. Cortex
Practical aspects of conducting large-scale functional magnetic resonance imaging studies in children
J. Child Neurol.
A developmental functional MRI study of prefrontal activation during performance of a go–no-go task
J. Cogn. Neurosci.
Dissociating striatal and hippocampus function developmentally with a stimulus–response compatibility task
J. Neurosci.
Quantitative morphology of the caudate nucleus in attention deficit hyperactivity disorder
Am. J. Psychiatry
Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder
JAMA
The human brain age 7–11 years: a volumetric analysis based on magnetic resonance images
Cereb. Cortex
Changes in regional cerebral blood flow during brain maturation in children and adolescents
J. Nucl. Med.
The lennox-gastaut syndrome: metabolic subtypes determined by 2-deoxy-2[18f]fluoro-d-glucose positron emission tomography
Ann. Neurol.
The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients
Brain
Cited by (63)
Experience-dependent neurodevelopment of self-regulation in adolescence
2024, Developmental Cognitive NeuroscienceAtypical language representation in children with intractable temporal lobe epilepsy
2016, Epilepsy and BehaviorDevelopmental Dyscalculia and the Brain
2015, Development of Mathematical Cognition: Neural Substrates and Genetic Influences: Volume 2The development of the neural substrates of cognitive control in adolescents with autism spectrum disorders
2014, Biological PsychiatryCitation Excerpt :Although relatively little is known about developmental neuropathology in ASD, early brain overgrowth (92) and neurobiological insults (93–95) may set the stage for atypical patterns of adolescent maturation of neural circuits such that there are base rate reductions in frontoparietal connectivity that produce sustained overconnectivity in nodes of the typical reactive control network. This would constitute a regionally weighted compensatory strategy according to Just et al. (56) and Berl et al. (91). Indeed, there now are several studies suggesting atypical functioning of the ACC in adults with ASD.
- ☆
Presented at the International Neuropsychological Society 2004.