The developmental cognitive neuroscience of functional connectivity

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.

[1]  J. Sweeney,et al.  The Emergence of Collaborative Brain Function: fMRI Studies of the Development of Response Inhibition , 2004, Annals of the New York Academy of Sciences.

[2]  T. Klingberg,et al.  Maturation of White Matter is Associated with the Development of Cognitive Functions during Childhood , 2004, Journal of Cognitive Neuroscience.

[3]  Changsong Zhou,et al.  Hierarchical organization unveiled by functional connectivity in complex brain networks. , 2006, Physical review letters.

[4]  Antigona Martinez,et al.  Early development of subcortical regions involved in non-cued attention switching. , 2004, Developmental science.

[5]  Ulrich Müller,et al.  The development of executive function in early childhood: I. The development of executive function. , 2003 .

[6]  Christian Büchel Perspectives on the estimation of effective connectivity from neuroimaging data , 2007, Neuroinformatics.

[7]  S. Reimers,et al.  Task switching across the life span: effects of age on general and specific switch costs. , 2005, Developmental psychology.

[8]  T. Klingberg Development of a superior frontal–intraparietal network for visuo-spatial working memory , 2006, Neuropsychologia.

[9]  J. Kelso,et al.  Cortical coordination dynamics and cognition , 2001, Trends in Cognitive Sciences.

[10]  M. Just,et al.  fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. , 2008, Cerebral cortex.

[11]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[12]  M. Reiff,et al.  Maturation of brain function associated with response inhibition. , 2003 .

[13]  B. Kolb Overview of cortical plasticity and recovery from brain injury. , 2003, Physical medicine and rehabilitation clinics of North America.

[14]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

[15]  P. Anderson Assessment and Development of Executive Function (EF) During Childhood , 2002, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[16]  T. Hare,et al.  Changes in cerebral functional organization during cognitive development , 2005, Current Opinion in Neurobiology.

[17]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[18]  Barry Horwitz,et al.  Relating fMRI and PET signals to neural activity by means of large-scale neural models , 2007, Neuroinformatics.

[19]  Converging methods in developmental science: an introduction. , 2002, Developmental psychobiology.

[20]  A. Diamond Developmental Time Course in Human Infants and Infant Monkeys, and the Neural Bases of, Inhibitory Control in Reaching a , 1990, Annals of the New York Academy of Sciences.

[21]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[22]  Donald T. Stuss,et al.  Biological and psychological development of executive functions , 1992, Brain and Cognition.

[23]  Geoffrey Bird,et al.  Attention does not modulate neural responses to social stimuli in autism spectrum disorders , 2006, NeuroImage.

[24]  B. J. Casey,et al.  What have we learned about cognitive development from neuroimaging? , 2006, Neuropsychologia.

[25]  B. Ambridge,et al.  The structure of working memory from 4 to 15 years of age. , 2004, Developmental psychology.

[26]  B. J. Casey,et al.  Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[27]  Daniel P. Kennedy,et al.  The intrinsic functional organization of the brain is altered in autism , 2008, NeuroImage.

[28]  James R. Booth,et al.  Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands , 2008, Brain Research.

[29]  Karl J. Friston,et al.  Modelling functional integration: a comparison of structural equation and dynamic causal models , 2004, NeuroImage.

[30]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[31]  Habib Benali,et al.  Regions, systems, and the brain: Hierarchical measures of functional integration in fMRI , 2008, Medical Image Anal..

[32]  M. P. van den Heuvel,et al.  Normalized Cut Group Clustering of Resting-State fMRI Data , 2008, PloS one.

[33]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[34]  M. Mehta Neuronal Dynamics of Predictive Coding , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[35]  Karl J. Friston,et al.  Modelling event-related responses in the brain , 2005, NeuroImage.

[36]  J. Fuster The cognit: a network model of cortical representation. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[37]  L. Steinberg Cognitive and affective development in adolescence , 2005, Trends in Cognitive Sciences.

[38]  A. Kramer,et al.  Changes in executive control across the life span: examination of task-switching performance. , 2001, Developmental psychology.

[39]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[40]  V. Calhoun,et al.  Functional neural circuits for mental timekeeping , 2007, Human brain mapping.

[41]  R. McKinstry,et al.  Diffusion tensor imaging and tractography of human brain development. , 2006, Neuroimaging clinics of North America.

[42]  Rajan S. Patel,et al.  A Bayesian approach to determining connectivity of the human brain , 2006, Human brain mapping.

[43]  Geraldine Dawson,et al.  Abnormal functional connectivity in autism spectrum disorders during face processing. , 2008, Brain : a journal of neurology.

[44]  Karl J. Friston,et al.  Dynamic causal models of neural system dynamics: current state and future extensions , 2007, Journal of Biosciences.

[45]  E. Bullmore,et al.  Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI , 2000, Neuroscience & Biobehavioral Reviews.

[46]  T. Shultz,et al.  Modeling developmental cognitive neuroscience , 2006, Trends in Cognitive Sciences.

[47]  A. Fingelkurts,et al.  Functional connectivity in the brain—is it an elusive concept? , 2005, Neuroscience & Biobehavioral Reviews.

[48]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[49]  Jérémie Mattout,et al.  Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework , 2007, NeuroImage.

[50]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[51]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[52]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[53]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[54]  Dietrich Lehmann,et al.  Millisecond by Millisecond, Year by Year: Normative EEG Microstates and Developmental Stages , 2002, NeuroImage.

[55]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[56]  Douglas C. Noll,et al.  A Developmental Functional MRI Study of Spatial Working Memory , 1999, NeuroImage.

[57]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[58]  M. Coles Preparation, sensory-motor interaction, response evaluation, and event-related brain potentials , 1998 .

[59]  Jos J. Eggermont,et al.  Neural connectivity only accounts for a small part of neural correlation in auditory cortex , 1996, Experimental Brain Research.

[60]  William Davis Gaillard,et al.  Developmental Aspects of Pediatric fMRI: Considerations for Image Acquisition, Analysis, and Interpretation , 2001, NeuroImage.

[61]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[62]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[63]  Ying Guo,et al.  Statistical approaches to functional neuroimaging data. , 2007, Neuroimaging clinics of North America.

[64]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[65]  C. Shatz,et al.  Brain Waves and Brain Wiring: The Role of Endogenous and Sensory-Driven Neural Activity in Development , 1999, Pediatric Research.

[66]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[67]  Vince D. Calhoun,et al.  Investigation of relationships between fMRI brain networks in the spectral domain using ICA and Granger causality reveals distinct differences between schizophrenia patients and healthy controls , 2009, NeuroImage.

[68]  D. Amso,et al.  Contributions of Neuroscience to Our Understanding of Cognitive Development , 2008, Current directions in psychological science.

[69]  Cecil R. Reynolds,et al.  A Model of the Development of Frontal Lobe Functioning: Findings From a Meta-Analysis , 2005, Applied neuropsychology.

[70]  Thomas R. Knösche,et al.  Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control , 2005, Journal of Cognitive Neuroscience.

[71]  M. Brammer,et al.  Progressive increase of frontostriatal brain activation from childhood to adulthood during event‐related tasks of cognitive control , 2006, Human brain mapping.

[72]  Karl J. Friston,et al.  PHRENOLOGY : What Can Neuroimaging Tell Us About Distributed Circuitry ? , 2005 .

[73]  Michael S. Gazzaniga,et al.  Functional Connectivity: Integrating Behavioral, Diffusion Tensor Imaging, and Functional Magnetic Resonance Imaging Data Sets , 2005, Journal of Cognitive Neuroscience.

[74]  D. Amso,et al.  Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching , 2006, Neuropsychologia.

[75]  Jeong‐Wook Ghim,et al.  Learning-Induced Enduring Changes in Functional Connectivity among Prefrontal Cortical Neurons , 2007, The Journal of Neuroscience.

[76]  C. Nelson Brain Development during Puberty and Adolescence: Comments on Part II , 2004, Annals of the New York Academy of Sciences.

[77]  Barry Horwitz,et al.  The elusive concept of brain connectivity , 2003, NeuroImage.

[78]  T. Klingberg,et al.  Increased prefrontal and parietal activity after training of working memory , 2004, Nature Neuroscience.

[79]  M. Hogge,et al.  Exploration of the neural substrates of executive functioning by functional neuroimaging , 2006, Neuroscience.

[80]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[81]  Vince D. Calhoun,et al.  Functional neural networks underlying response inhibition in adolescents and adults , 2007, Behavioural Brain Research.

[82]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[83]  James R. Booth,et al.  Neural development of selective attention and response inhibition , 2003, NeuroImage.

[84]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

[85]  Karl J. Friston,et al.  Extra-classical receptive field effects measured in striate cortex with fMRI , 2007, NeuroImage.

[86]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Ch. von der Malsburg,et al.  A neural cocktail-party processor , 1986, Biological Cybernetics.

[88]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[89]  P. Nunez Toward a quantitative description of large-scale neocortical dynamic function and EEG , 2000, Behavioral and Brain Sciences.

[90]  J. C. Jimenez,et al.  Nonlinear local electrovascular coupling. I: A theoretical model , 2006, Human brain mapping.

[91]  Timothy Edward John Behrens,et al.  New approaches for exploring anatomical and functional connectivity in the human brain , 2004, Biological Psychiatry.

[92]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[93]  D. Tucker,et al.  Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. , 2000, Journal of experimental psychology. General.

[94]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[95]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[96]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[97]  S. Bressler,et al.  Operational principles of neurocognitive networks. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[98]  Vicki A. Anderson,et al.  Development of Executive Functions Through Late Childhood and Adolescence in an Australian Sample , 2001, Developmental neuropsychology.

[99]  Deborah A Yurgelun-Todd,et al.  Cognitive and Emotional Components of Frontal Lobe Functioning in Childhood and Adolescence , 2004, Annals of the New York Academy of Sciences.

[100]  G. Gratton,et al.  Combining structural and functional neuroimaging data for studying brain connectivity: a review. , 2008, Psychophysiology.

[101]  Mark H. Johnson Functional brain development in humans , 2001, Nature Reviews Neuroscience.

[102]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[103]  R. J. MacGregor,et al.  Characterization, scaling, and partial representation of neural junctions and coordinated firing patterns by dynamic similarity , 1995, Biological Cybernetics.

[104]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[105]  T. Paus Mapping brain maturation and cognitive development during adolescence , 2005, Trends in Cognitive Sciences.

[106]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[107]  Giulio Tononi,et al.  Integrated Information in Discrete Dynamical Systems: Motivation and Theoretical Framework , 2008, PLoS Comput. Biol..

[108]  Vincent Schmithorst,et al.  Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis , 2007, NeuroImage.

[109]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[110]  Olaf Sporns,et al.  Connectivity and complexity: the relationship between neuroanatomy and brain dynamics , 2000, Neural Networks.

[111]  Caroline C Brown,et al.  Disordered connectivity in the autistic brain: challenges for the "new psychophysiology". , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[112]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[113]  A. Seth Causal connectivity of evolved neural networks during behavior. , 2005, Network.

[114]  K. Jellinger Processes of Change in Brain and Cognitive Development Attention and Performance XXI , 2007 .

[115]  Stefan Wermter,et al.  A hybrid generative and predictive model of the motor cortex , 2006, Neural Networks.

[116]  D. Barth,et al.  Submillisecond Synchronization of Fast Electrical Oscillations in Neocortex , 2003, The Journal of Neuroscience.

[117]  R. Malenka,et al.  Synaptic Plasticity: Multiple Forms, Functions, and Mechanisms , 2008, Neuropsychopharmacology.

[118]  F. Bartolomei,et al.  Imaging structural and functional connectivity: towards a unified definition of human brain organization? , 2008, Current opinion in neurology.

[119]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[120]  James R. Booth,et al.  Developmental changes in activation and effective connectivity in phonological processing , 2007, NeuroImage.

[121]  P S Goldman-Rakic,et al.  Development of cortical circuitry and cognitive function. , 1987, Child development.

[122]  Karl J. Friston,et al.  Generative models, brain function and neuroimaging. , 2001, Scandinavian journal of psychology.

[123]  Michael S. C. Thomas,et al.  Atypical representational change: conditions for theemergence of atypical modularity , 2006 .

[124]  Mark Tommerdahl,et al.  Absence of stimulus-driven synchronization effects on sensory perception in autism: Evidence for local underconnectivity? , 2008, Behavioral and Brain Functions.

[125]  V Menon,et al.  Maturation of medial temporal lobe response and connectivity during memory encoding. , 2005, Brain research. Cognitive brain research.

[126]  T. Sejnowski,et al.  Irresistible environment meets immovable neurons , 1997, Behavioral and Brain Sciences.

[127]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[128]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[129]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[130]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[131]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: I. Increases in Subcortical Structures and Cerebellum but Not in Nonvisual Cortex , 1997, Journal of Cognitive Neuroscience.

[132]  Anne Caclin,et al.  Effect of initial fMRI data modeling on the connectivity reported between brain areas , 2006, NeuroImage.

[133]  M. Sommer,et al.  Corollary discharge across the animal kingdom , 2008, Nature Reviews Neuroscience.

[134]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[135]  M. Tosetti,et al.  Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling , 2007, Journal of magnetic resonance imaging : JMRI.

[136]  Tali Bitan,et al.  The interaction between orthographic and phonological information in children: An fMRI study , 2007, Human brain mapping.

[137]  P. Goldman-Rakic,et al.  Development of the prefrontal cortex : evolution, neurobiology, and behavior , 1997 .

[138]  S. Blakemore,et al.  Development of the adolescent brain: implications for executive function and social cognition. , 2006 .

[139]  V. Calhoun,et al.  Brain network dynamics during error commission , 2009, Human brain mapping.

[140]  Febo Cincotti,et al.  Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis. , 2004, Behavioral neuroscience.

[141]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[142]  Yihong Yang,et al.  A neural basis for the development of inhibitory control , 2002 .

[143]  Conor V. Dolan,et al.  Source (or Part of the following Source): Type Article Title Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis Author(s) Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis , 2022 .

[144]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[145]  G. Ramakers,et al.  Neuronal network formation in human cerebral cortex. , 2005, Progress in brain research.

[146]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[147]  Jeffrey D. Riley,et al.  Neuroplasticity and brain repair after stroke , 2008, Current opinion in neurology.

[148]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[149]  Fivos Panetsos,et al.  A method for determining neural connectivity and inferring the underlying network dynamics using extracellular spike recordings , 2005, Journal of Neuroscience Methods.

[150]  Andreas A Ioannides,et al.  Dynamic functional connectivity , 2007, Current Opinion in Neurobiology.

[151]  H. Berendse,et al.  The application of graph theoretical analysis to complex networks in the brain , 2007, Clinical Neurophysiology.

[152]  G. Edelman,et al.  Complexity and coherency: integrating information in the brain , 1998, Trends in Cognitive Sciences.

[153]  A. McIntosh,et al.  Mapping cognition to the brain through neural interactions. , 1999, Memory.

[154]  D. Yves von Cramon,et al.  Neuroimaging of Performance Monitoring: Error Detection and Beyond , 2004, Cortex.

[155]  Y. Munakata,et al.  Developmental cognitive neuroscience: progress and potential , 2004, Trends in Cognitive Sciences.

[156]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[157]  Deanna Kuhn,et al.  Do Cognitive Changes Accompany Developments in the Adolescent Brain? , 2006, Perspectives on psychological science : a journal of the Association for Psychological Science.

[158]  Dietmar Cordes,et al.  Hierarchical clustering to measure connectivity in fMRI resting-state data. , 2002, Magnetic resonance imaging.

[159]  J. Henson,et al.  Plasticity , 2010, Neurology.

[160]  E. Martin,et al.  Functional MR imaging in pediatrics. , 2001, Magnetic resonance imaging clinics of North America.

[161]  John C Gore,et al.  Assessing functional connectivity in the human brain by fMRI. , 2007, Magnetic resonance imaging.