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Developmental Pathways to Functional Brain Networks: Emerging Principles

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Developmental Pathways to Functional Brain Networks: Emerging Principles TICS-1251; No. of Pages 14 Review Special Issue: The Connectome Developmental pathways to functional brain networks: emerging principles 1,2,3 V. Menon 1 Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA 94304, USA 2 Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA 94304, USA 3 Program in Neuroscience, Stanford University School of Medicine, Stanford, CA 94304, USA The human brain undergoes protracted developmental disorders. The perspective advanced in this review is that changes during which it constructs functional networks a thorough understanding of the functional architecture of that engender complex cognitive abilities. Understand- the adult brain requires critical consideration of the devel- ing brain function ultimately depends on knowledge of opmental pathways by which plasticity and learning lead how dynamic interactions between distributed brain to the construction of dedicated large-scale brain systems. regions mature with age to produce sophisticated cog- Most, if not all, major psychopathologies, with the excep- nitive systems. This review summarizes recent progress tion of the dementias, have a prominent origin in childhood in our understanding of the ontogeny of functional brain or adolescence [4]. The onset and diagnosis of these psycho- networks. Here I describe how complementary methods pathologies vary greatly: some, like autism, are mainly for probing functional connectivity are providing unique diagnosed in early childhood, others such as attention deficit insights into the emergence and maturation of distinct hyperactivity disorder and anxiety disorders are mainly functional networks from childhood to adulthood. diagnosed in middle childhood, whereas bipolar disorder, I highlight six emerging principles governing the devel- depression, and schizophrenia are predominantly diag- opment of large-scale functional networks and discuss nosed in late adolescence. For the past two decades, struc- how they inform cognitive and affective function in tural brain imaging, with an emphasis on gray matter typically developing children and in children with neu- volume, was the mainstay for identifying abnormalities in rodevelopmental disorders. children and adolescents with these disorders. An important limitation of these studies is that they provide a relatively Cognitive development from the perspective of narrow window into the distributed functional systems functional brain networks impacted in psychopathology. A paradigm shift is now The emergence of complex cognitive functions, such as language, reasoning, and cognitive control, is a hallmark of human development [1]. These extraordinary and Glossary uniquely human abilities are made possible by a protracted Attention deficit hyperactivity disorder: one of the most common childhood trajectory of brain development and learning over the first disorders that can continue through adolescence and adulthood. Symptoms two decades of life [2]. Understanding how the developing include difficulty staying focused and paying attention, difficulty controlling behavior, and hyperactivity. brain achieves such abilities ultimately depends on knowl- Autism: a neurodevelopmental disorder that appears in the first 3 years of life edge of how functional interactions between distributed and affects normal development of social and communication skills. Indivi- brain regions mature with age to produce sophisticated duals with autism have difficulties with social interaction, display problems with verbal and nonverbal communication, and exhibit repetitive behaviors or cognitive systems. Brain network analyses are increasing- narrow, obsessive interests. ly being used to characterize the developing brain and to Central executive network (CEN): a brain network that is responsible for high- level cognitive functions such as planning, decision making, and the control of understand the dynamic maturation processes that engen- attention and working memory. der complex human cognitive abilities [3]. New research is Default mode network (DMN): a large-scale network of brain areas that form an beginning to demonstrate how functional brain networks integrated system for self-related mental activity, including autobiographical, self-monitoring, and social functions. The DMN is typically deactivated during emerge from childhood to adulthood, providing fundamen- stimulus-driven cognitive processing. tal new insights not only into the ontogeny of complex brain Graph-theoretical measures: a graph is a mathematical structure comprising function in typically developing individuals, but also into nodes and the edges that connect them. Expressing functional brain connectivity as a graph allows quantitative association of network properties the processes that can go awry in neurodevelopmental such as path length, clustering, degree, modularity, and hierarchy. Intrinsic functional connectivity: a measure of spontaneous synchronization of brain signals between two or more areas. It is computed using the statistical Corresponding author: Menon, V. ([email protected]). relation of temporal changes in different brain areas in the absence of external 1364-6613/$ – see front matter stimuli i.e., (‘rest’). ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tics.2013.09.015 Salience network (SN): a large-scale brain network involved in detecting and orienting to salient external stimuli and internal events. Small-world network: a network in which most nodes are not neighbors of one another, but most nodes can be reached from every other node with a small number of links. Small-world networks optimize wiring and efficiency. Trends in Cognitive Sciences xx (2013) 1–14 1 TICS-1251; No. of Pages 14 Review Trends in Cognitive Sciences xxx xxxx, Vol. xxx, No. x emerging in the study of neurodevelopmental disorders in Box 1. Six emerging principles of functional brain network children, propelled by recent conceptual and methodological development advances in characterizing brain networks and connectivity [5–10]. Critically, this research is also leading to a more (i) Small-world, hierarchical organization and formation of hubs. thorough characterization of aberrant brain development Functional brain networks are constructed from an anatomical and providing complementary biological markers for early backbone that is mature by age 2. Key topological features of global functional brain architecture are mature by age 8, but detection and classification of neurodevelopmental disor- large-scale functional brain connectivity continues to undergo ders [11–13]. significant restructuring during late childhood and adolescence, In this review, I outline a developmental perspective on leading to the emergence of a hierarchical brain organization functional brain networks and discuss how advances in our and formation of functional hubs that integrate complex understanding of typical and atypical brain connectivity in exogenous and endogenous mental processes. (ii) Segregation of functional circuits. Development is characterized children and adolescents are providing new insights into by increased segregation of functional brain circuits, with a shift the construction of mature functional systems in adults. I from stronger short-range connections in children to stronger first present a brief overview of methodological and con- and more distinct patterns long-range connections in adults. ceptual issues involved in characterizing brain systems in This pattern is observed at multiple spatial scales, including global architecture, functional subsystems, and individual typical and atypical development, pointing out the unique cytoarchitectonically distinct nuclei. insights afforded by different analytic approaches. I then (iii) Changing landscape of subcortical–cortical functional connec- examine the global architecture of the developing brain, tivity. Reconfiguration of subcortical–cortical connections is a focusing on the development of a small-world organization, major hallmark of functional brain network development. In the changing landscape of subcortical–cortical interac- particular, basal ganglia–cortical circuits important for motiva- tion, reward- and incentive-based learning, and habit formation tions, and the emergence of segregated circuits as key undergo significant changes between childhood and adulthood. features of the maturing functional architecture between Aberrant development of subcortical–cortical connectivity plays infancy and adulthood. I describe several key intrinsic an important role in several major neurodevelopmental dis- neurocognitive networks that play distinct roles in cogni- orders including autism and attention deficit hyperactivity tion, highlighting how they are reconfigured in typical disorder. (iv) Dynamic pruning of functional circuits. The dynamic process of development and the implications of these dynamic over-connectivity followed by pruning, which rewires connec- changes for understanding cognitive function. Aberrations tions at the synaptic level, also operates at the systems level, in the development of these networks and how they con- helping to reconfigure and rebalance connectivity in the tribute to psychopathology and clinical symptoms are then developing brain. examined using examples from major neurodevelopmental (v) Reconfiguration of large-scale functional networks. Functional connectivity within and between spatially independent large- disorders including
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