Cited by 411Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsAdvanced MRI Techniques and Applications

Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature

Open access
Grayson, David S., Fair, Damien A.·2017·NeuroImage

Abstract

The development of human cognition results from the emergence of coordinated activity between distant brain areas. Network science, combined with non-invasive functional imaging, has generated unprecedented insights regarding the adult brain's functional organization, and promises to help elucidate the development of functional architectures supporting complex behavior. Here we review what is known about functional network development from birth until adulthood, particularly as understood through the use of resting-state functional connectivity MRI (rs-fcMRI). We attempt to synthesize rs-fcMRI findings with other functional imaging techniques, with macro-scale structural connectivity, and with knowledge regarding the development of micro-scale structure. We highlight a number of outstanding conceptual and technical barriers that need to be addressed, as well as previous developmental findings that may need to be revisited. Finally, we discuss key areas ripe for future research in order to (1) better characterize normative developmental trajectories, (2) link these trajectories to biologic mechanistic events, as well as component behaviors and (3) better understand the clinical implications and pathophysiological basis of aberrant network development.

Integrity signals

Registry

Crossref · 10.1016/j.neuroimage.2017.01.079

Cites

211 of 211 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

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  • Premisecitation

    Resting-state networks are highly reproducible in the adult brain.

    “RSNs have proven to be highly reproducible in the adult brain (Doucet et al., 2011; Gordon et al., 2016; Power et al., 2011; Yeo et al., 2011)”
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    Neonatal hubs primarily involve early sensorimotor, visual, and limbic regions.

    “whereas neonatal hubs primarily involve early sensorimotor, visual, and limbic regions (De Asis-Cruz et al., 2015; Fransson et al., 2011; Gao et al., 2011).”
    • Also stated in: § Regional hub metrics · plain
      “whereas neonatal hubs primarily involve early sensorimotor, visual, and limbic regions (De Asis-Cruz et al., 2015; Fransson et al., 2011; Gao et al., 2011)”
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  • Premisecitation

    Functional connectivity patterns within and between major resting-state networks are associated with task-relevant behavioral performance.

    “and are associated with task-relevant behavioral performance (Cole et al., 2012; Lewis et al., 2009).”
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  • Interpretationcitation

    Functional connectivity aberrations may indicate the etiological bases of neuropsychiatric disorders.

    “and that FC aberrations may point towards the etiological bases of neuropsychiatric disorders (e.g. (Swartz and Monk, 2014; van den Heuvel et al., 2016a)).”
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  • Premisecitation

    Individual cognitive abilities generally depend on distributed networks rather than one localized region.

    “First, most individual cognitive abilities arise not solely from a particular brain area, but from networks of activity spanning multiple distributed regions (Petersen and Sporns, 2015).”
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    Premisecitation

    Small-worldness, global efficiency, and average clustering coefficient are already high in neonates.

    “Small-worldness (De Asis-Cruz et al., 2015; Fransson et al., 2011; Gao et al., 2011), as well as its constituent properties of global efficiency and average clustering coefficient, are already high in neonates.”
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    Premisecitation

    Later studies found comparable bilateral correlations in early visual and early auditory cortex.

    “followed soon after by similar findings of bilaterally correlated activity in early visual and early auditory cortex (Cordes et al., 2001; Kiviniemi et al., 2000; Lowe et al., 1998).”
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    Premisecitation

    Independent component analysis reliably identifies early visual, early auditory, and primary sensory/motor maps, along with distributed association-cortex components.

    “ICA maps reproducibly reveal early visual, early auditory, and primary sensory/motor components, as well as other components comprising distributed portions of the frontal, parietal, and temporal association cortices (Damoiseaux et al., 2006).”
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    Premisecitation

    Interregional functional connectivity arises from anatomical projection strengths, correlated gene expression, and synaptic receptor densities.

    “Interregional FC arises from anatomical projection strengths (Messe et al., 2014; Shen et al., 2012), correlated gene expression (Richiardi et al., 2015), and synaptic receptor densities (Turk et al., 2016; van den Heuvel et al., 2016b)”
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    Premisecitation

    The first observation of correlated resting-state activity was in bilateral sensorimotor cortex.

    “Correlated resting-state activity was first identified in bilateral sensorimotor cortex by (Biswal et al., 1995)”
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    Premisecitation

    Small-world organization appears across brain scales and is proposed to reflect a biological compromise between efficient integration and the expense of long-distance connections.

    “This property, which is ubiquitous across vastly different scales of investigation in the brain, is thought to emerge from a biological need to balance the benefits of integration against the costs of long-range wiring (Collin et al., 2013; Vertes and Bullmore, 2015).”
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    Interpretationcitation

    The observed sequence fits the presence of basic touch and vision at birth and findings that primary sensory cortex matures earliest.

    “These trends are consistent with the presence of basic somatosensory and visual functions at birth, and help contextualize findings that primary sensory regions are generally the first cortical areas to reach plateaus or peaks in growth (Geng et al., 2016; Gilmore et al., 2012; Lyall et al., 2015; Scott et al., 2015).”
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    Premisecitation

    Rich-club nodes tend to span multiple resting-state networks, aiding integration among them.

    “Rich-club nodes tend to span multiple RSNs, thereby facilitating integration between them (Sporns, 2013; van den Heuvel and Sporns, 2013).”
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    Premisecitation

    During the first two years, sensory networks mature and strengthen, becoming substantially adult-like by age two.

    “These sensory networks undergo subtle refinements and strengthening over the first two years of life, and by age two bear substantial resemblance to their adult counterparts (Gao et al., 2015a; Lin et al., 2008).”
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    Premisecitation

    At age two, the default-mode network resembles the adult form, but long-range anterior-posterior coupling is still relatively weak.

    “By two years of age, the network bears adult-like qualities, although coupling between distant anterior and posterior nodes of the network remain relatively low.”
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    Premisecitation

    The default-mode network is viewed as task-negative, associated with internal thought, and shows reduced activity during external tasks.

    “the DMN is considered “task-negative” as it has been linked to internal mentation and is known to deactivate during processing of external stimuli (Buckner et al., 2008)”
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    Premisecitation

    Resting-state networks are present in infancy and possibly to some degree before birth.

    “RSNs are already present during infancy, and potentially to some extent in utero (Thomason et al., 2013).”
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    Premisecitation

    Segregation and integration together are involved in cognitive control and executive function, and relate differently to simple motor versus complex working memory performance.

    “Both effects in tandem are crucially involved in cognitive control (Dwyer et al., 2014) and executive functioning (Reineberg et al., 2015), and are differentially associated with performance on simple motor tasks versus complex working memory tasks (Cohen and D’Esposito, 2016).”
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    Premisecitation

    Default-mode network subregions in neonates and young infants are locally correlated but not yet synchronized as one coherent network.

    “In neonates and very young infants, these individual compartments demonstrate locally correlated activity, but fail to synchronize into a coherent network (Damaraju et al., 2014; Fransson et al., 2007; Gao et al., 2009; Smyser et al., 2010; Wylie et al., 2014).”
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    Premisecitation

    Adult modular organization includes separate sensory/motor systems and the default-mode network.

    “These modules include 1) segregated, non-distributed modules for sensory/motor activity, such as in early visual cortex and in somatomotor cortex, 2) the default-mode network (DMN), comprising the medial prefrontal, posterior cingulate/precuneus, angular gyrus, and medial temporal cortex”
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    Premisecitation

    The brain doubles in volume during year one and attains 80-90% of adult size by age three.

    “doubling in volume during the first year and reaching 80–90% of adult volume by age 3 (Courchesne et al., 2000; Knickmeyer et al., 2008).”
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    Premisecitation

    Major fiber pathways are consolidated by myelination, but they are largely present before birth.

    “The brain’s major fiber pathways become consolidated through myelination, though their presence is largely established prenatally (Stiles and Jernigan, 2010).”
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    Interpretationreasoning

    Normal and pathological developmental changes in functional connectivity are best interpreted using an integrated structural-functional network approach.

    “By extension, one could reason that developmental modifications in brain FC, whether normative or pathological, are also best understood via an emerging network science that merges structural and functional connectivity data.”
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    Premisecitation

    The first years include widespread rapid synapse formation, then a long phase of synapse removal and cell loss that extends into adulthood.

    “This same time period is marked by rapid and widespread cortical synaptogenesis, followed by a protracted period of synapse elimination and cell loss which carries into adulthood (Huttenlocher, 2002; Innocenti and Price, 2005).”
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    Premisecitation

    Two-year-olds show separate auditory, sensorimotor, and visual modules, and perhaps early versions of salience, frontoparietal, and default-mode networks.

    “Community structure assessed at two years of age (Alcauter et al., 2015b; Gao et al., 2015b) indicates the presence of distinct modules encompassing early auditory, early somatomotor, and early visual areas, and potentially, other prototypical modules similar to the canonical salience, frontoparietal, and DMN seen in adults.”
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    Premisecitation

    Long-distance links are preferentially strengthened during the first year and level off thereafter.

    “Concomitantly, long-distance links are preferentially strengthened during the first year of life, leveling off thereafter (Gao et al., 2011).”
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    Study design and conductreasoning

    Early postnatal changes in cerebral vasculature and altered state of consciousness when scanning very young participants are considerations in infant rs-fcMRI.

    “Other considerations include early postnatal changes in cerebral vasculature, and altered state of consciousness when scanning very young participants.”
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    Premisecitation

    Prior to 2012, multiple studies found that functional connectivity between anatomically proximate ROIs gradually decreased, while long-range functional connections, especially anterior-posterior links, gradually increased until adulthood.

    “Prior to 2012, multiple studies had found that functional connectivity between anatomically proximate ROIs gradually decreased, whereas long-range functional connections, especially anterior-posterior links, gradually increased until adulthood (Dosenbach et al., 2010; Fair et al., 2009; Kelly et al., 2009; Supekar et al., 2009).”
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    Study design and conductcitation

    Different community detection algorithms can provide unique results and not all are appropriate for any given experimental condition.

    “different community detection algorithms can provide unique results and all are not appropriate for any given experimental condition (Gates et al., 2016).”
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    Premisecitation

    From birth through the first two years of life, synchronization and homotopic coupling increase while between-module connectivity decreases, indicating greater functional specialization.

    “synchronization and homotopic coupling from birth through the first two years of life (Gao et al., 2015b; Homae et al., 2010), concomitant with decreasing between-module connectivity (i.e. greater functional specialization).”
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    Study design and conductnone given

    Natural sleep or sedation attenuates micromovements and their attendant signal artifacts.

    “A natural benefit is the attenuation of micromovements and their attendant signal artifacts.”
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    Premisecitation

    A recent study using matched methods in adults and 1-2 year olds first directly showed many localized infant modules and how they map onto adult organization.

    “One recent report compared community structure in adults against that in 1–2 year olds using closely matched methods (Eggebrecht et al., 2017), providing the first direct evidence for numerous anatomically localized modules in the infant brain and their relationship to adult functional organization (Figure 2C).”
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    Premisecitation

    Rich clubs are evident in both structural and functional networks in neonates, along with high functional modularity and integration capacity between modules.

    “Rich clubs are also evident in both structural and functional networks in neonates along with both high functional modularity and integration capacity between modules (Ball et al., 2014; Scheinost et al., 2016a; van den Heuvel et al., 2015b).”
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    Interpretationcitation

    Anatomical areas involved in integrating different information processing streams are likely critical for complex cognitive and social abilities and potentially uniquely susceptible to early environmental influences.

    “Such anatomical areas are likely critical for the development of complex cognitive and social abilities, and are potentially uniquely susceptible to early environmental influences (Graham et al., 2015).”
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    Premisecitation

    From birth through age two, these modules markedly increase distributed synchronization and homotopic coupling.

    “These latter modules also exhibit substantial growth of distributed synchronization and homotopic coupling from birth through the first two years of life (Gao et al., 2015b; Homae et al., 2010), concomitant”
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    Premisecitation

    These properties marginally increase during the first year and plateau until at least the end of the second year.

    “These properties only appear to marginally increase during the first year of life, plateauing thereafter until at least the end of the second year (Gao et al., 2011).”
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    Premisecitation

    During the first two years, hubness of sensorimotor areas gradually decreases and involvement of association cortical areas increases, especially medial frontal and parietal default mode portions.

    “The first two years of life reflect a gradual decrease in the hubness of sensorimotor areas and increased involvement of various association cortical areas, especially the medial frontal and parietal portions of the default mode (Gao et al., 2011).”
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    Premisecitation

    The DMN exhibits increasingly synchronized within-network and between-network connections.

    “The DMN was found to exhibit both increasingly synchronized within-network and between-network connections.”
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    Premisecitation

    Among cortical areas, some report increasing hubness of frontal nodes, while other lobes show mixed reports of increasing, decreasing, or stable hubness.

    “Among cortical areas, some have reported increasing hubness of frontal nodes (Cao et al., 2014; Wu et al., 2013) while in other lobes there have been mixed reports of increasing (Cao et al., 2014; Grayson et al., 2014) and decreasing (Wu et al., 2013; Zuo et al., 2012), or stable (Hwang et al., 2013) hubness.”
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    Interpretationreasoning

    These trends pointed to dampening of non-specific local spread of activity and strengthening of long-range links, facilitating cognitive development through modular specialization and selective cross-network integration.

    “These trends pointed to coherent changes that involved a dampening of non-specific local spread of activity and strengthening of long-range links, facilitating cognitive development through modular specialization and selective cross-network integration (Bunge and Wright, 2007; Fair et al., 2009; Uddin, 2011; Uddin et al., 2011).”
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    Premisecitation

    Increased cross-network integration between cingulo-opercular/salience and somatomotor modules occurs over age 10-26 and is associated with cognitive control development.

    “Similar, albeit not identical developmental findings, are observed by (Marek et al., 2015)), who found increased cross-network integration between the cingulo-opercular/salience and somatomotor modules over the age of 10–26, which they showed to be associated with the development of cognitive control.”
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    Premisecitation

    Specific connections to cortical hub regions increase during childhood and adolescence, resulting in increased rich club coefficients in adulthood.

    “More detailed network analyses have revealed that specific connections to cortical hub regions increase during childhood and adolescence (Grayson et al., 2014; Hwang et al., 2013) resulting in increased rich club coefficients in adulthood (Cao et al., 2014; Grayson et al., 2014).”
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    Premisecitation

    Frontal and parietal cortical gray matter volume decreases across 5-30 years and exhibits curvilinear trajectories closely correlated with loss of slow-wave power in the same areas.

    “Interestingly, frontal and parietal cortical gray matter (but not white matter) volume decreases across this same age bracket, and exhibits curvilinear trajectories that are closely correlated to the loss of slow-wave power in these same areas (Buchmann et al., 2011; Smit et al., 2012; Whitford et al., 2007).”
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    Premisecitation

    Despite adult-like organization, refinements within and between systems occur over time.

    “Despite this “adult like” level of organization, refinements within and between systems does appear to occur over time, although details to this end are still being worked out (Fair et al., 2012b; Gu et al., 2015b; Marek et al., 2015).”
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    Premisecitation

    Two reports found path length increases with age, while more recent work demonstrates age-related reductions.

    “Somewhat unexpectedly, two reports found path length to also increase with age (Boersma et al., 2011; Smit et al., 2012), although more recent work demonstrates age-related reductions (Miskovic et al., 2015).”
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    Premisereasoning

    EEG/MEG resting-state networks provide greater temporal resolution than rs-fMRI and offer complementary insights about functional development.

    “Resting-state networks obtained using electrophysiological recording (EEG or MEG) provide greater temporal resolution (<100Hz) relative to rs-fMRI (<0.1Hz) and therefore offer complementary insights about functional development.”
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    Interpretationreasoning

    These mixed or non-significant findings might suggest that regional properties of cortical hubs are largely established during very early development.

    “At first glance, these mixed or non-significant findings might suggest that regional properties of cortical hubs are largely established during very early development.”
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    Interpretationreasoning

    Recent convergence of data suggests that network structure continues to evolve after late childhood in ways not primarily distance-dependent, with complex specific changes coinciding with development of specific cognitive abilities.

    “Therefore, there is recent convergence of data suggesting that network structure continues to evolve after late childhood in ways that are not primarily distance-dependent; rather, complex but specific changes may coincide with the development of specific cognitive abilities.”
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    Premisecitation

    Networks involved in task-positive cognitive function (salience, frontoparietal executive, attentional) became increasingly segregated and exhibited increasingly variable spatial structure.

    “On the other hand, networks involved in task-positive cognitive function (e.g. salience, frontoparietal executive, and attentional networks), being generally well-connected with other systems, became increasingly segregated and exhibited increasingly variable spatial structure.”
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    Study design and conductreasoning

    EEG/MEG studies are generally unable to map activity to precise brain areas due to source localization challenges and often treat scalp sensors as network nodes.

    “It is important to note that these studies are generally unable to map activity to precise brain areas due to challenges in source localization, and often treat the scalp sensors as the network nodes.”
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    Premisecitation

    Age-related changes in functional connectivity disproportionately impact polysynaptic connections, though the study spanned the lifespan and may reflect aging.

    “Another study found that age-related changes in FC disproportionately impacts polysynaptic connections (Betzel et al., 2014), although this study was performed across the lifespan and may reflect an effect of aging.”
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    Premisecitation

    Global signal regression is arguably the most effective motion-denoising technique currently available.

    “The most contentious debate probably concerns the use of global signal regression (GSR) – arguably the most effective motion-denoising technique currently available (Burgess et al., 2016; Power et al., 2015; Yan et al., 2013).”
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    Interpretationcitation

    Predictive models have been extensively validated on both rs-fcMRI and EEG data, suggesting that SC strongly shapes and constrains activity across temporal scales.

    “Predictive models have been extensively validated on both rs-fcMRI and EEG data (Chu et al., 2015), suggesting that SC strongly shapes and constrains activity across temporal scales.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Chu et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Over development, rs-fcMRI networks show increased within-subject variability, consistent with EEG studies showing increased signal complexity.

    “Over development, rs-fcMRI networks show increased within-subject variability (Hutchison and Morton, 2015; Marusak et al., 2016; Qin et al., 2015), consistent with EEG studies showing that signal complexity increases over development (McIntosh et al., 2008; Vakorin et al., 2011).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Hutchison and Morton, 2015

      Not checked in the free run.

    • cites Marusak et al., 2016

      Not checked in the free run.

    • cites Qin et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The highest reported correlation between monkey tract-tracer and tractography networks is r = 0.59, though it is often much lower.

    “Currently, the highest reported correlation stands at r = 0.59 (Donahue et al., 2016), though it is often much lower (van den Heuvel et al., 2015a).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Donahue et al., 2016 source

      Not checked in the free run.

    • cites van den Heuvel et al., 2015a

      Not checked in the free run.

  • May combine two claims.

    Study design and conductcitation

    Instability exists in the form of measurable state transitions (e.g., awake to sleep, eyes open versus closed), and there is considerably less evidence for intrinsic dynamics otherwise.

    “The authors note that instability is not absent, but that it exists in the form of measurable state transitions (e.g. from awake to sleep, or eyes open verus closed), and that there is considerably less evidence for intrinsic dynamics otherwise.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Laumann et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Head motion increases functional correlations between spatially proximal nodes and decreases correlations between distant nodes.

    “head motion increases functional correlations between spatially proximal nodes and decreases correlations between distant nodes (Power et al., 2012).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Power et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Schizophrenia, ADHD, Autism, and potentially other DSM-defined disorders each constitute a highly heterogeneous set of etiologies.

    “The first challenge is the ever-expanding evidence that Schizophrenia (Meda et al., 2014; Satterthwaite and Baker, 2015), ADHD (Costa Dias et al., 2015; Fair et al., 2012a; Gates et al., 2014; Karalunas et al., 2014), Autism (Jeste and Geschwind, 2014; Rudie et al., 2012), and potentially other DSM defined disorders, each constitutes a highly heterogeneous set of etiologies.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Meda et al., 2014 source

      Not checked in the free run.

    • cites Costa Dias et al., 2015 source

      Not checked in the free run.

    • cites Jeste and Geschwind, 2014 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    New multimodal approaches that anchor surface-based registrations to other structural or functional characteristics of an individual are likely to improve subject-to-subject registrations and reduce intersubject variability.

    “New multimodal approaches that also anchor surface-based registrations to other structural or functional characteristics of an individual are likely to improve subject to subject registrations, and hence reduce intersubject variability, even more (e.g.(Glasser et al., 2016b; Robinson et al., 2014).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Glasser et al., 2016b

      Not checked in the free run.

    • cites Robinson et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Probing cellular and molecular markers across the whole human brain at high-throughput is exceptionally difficult and cannot be done under strict experimental conditions.

    “probing cellular and molecular markers across the whole human brain at high-throughput is exceptionally difficult (Richiardi et al., 2015) and cannot be done under strict experimental conditions.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Richiardi et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given

    Community structure at birth is coarse and primitive, but gradually evolves into a denser, more spatially structured, and distributed organization.

    “Community structure at birth is coarse and primitive, but gradually evolves into a denser, more spatially structured, and distributed organization.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Tight control of functional imaging conditions was needed in Grayson et al. to reveal novel structure-function relationships and maximize model performance.

    “One interesting aspect of the work in (Grayson et al., 2016) is how tightly functional imaging conditions had to be controlled in order to reveal novel structure-function relationships and in order to maximize model performance”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Grayson et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Functional areas contain distinct combinations of inputs and outputs, which group related areas into specialized networks.

    “They also contain distinct combinations of inputs and outputs, which in turn group related areas into specialized networks (Felleman and Van Essen, 1991).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Felleman and Van Essen, 1991 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    FC networks in one highly sampled individual converged as a function of the timeseries length used to extract correlations and were extremely reproducible using approximately 1 hour of motion-free data.

    “FC networks in one highly sampled individual converged as a function of the timeseries length used to extract correlations and were extremely reproducible using approximately 1 hour of motion-free data (Laumann et al., 2015).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Laumann et al., 2015 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationnone given

    A very large portion of the current human developmental literature is in dire need of re-examination in light of recent developments regarding systematic artifacts in the imaging signals.

    “a very large portion of the current human developmental literature is in dire need of re-examination in light of recent developments regarding systematic artifacts in the imaging signals.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Global topological metrics for structural and functional networks show stability across different parcellation schema of similar density, but vary considerably as a function of network size.

    “Global topological metrics for structural and functional networks show stability across different parcellation schema of similar density, but vary considerably as a function of network size (de Reus and van den Heuvel, 2013; Fornito et al., 2010; Zalesky et al., 2010).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites de Reus and van den Heuvel, 2013 source

      Not checked in the free run.

    • cites Fornito et al., 2010

      Not checked in the free run.

    • cites Zalesky et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Motion artifacts appear to be tightly related to clinical factors and a whole host of behavioral phenotypes and metrics.

    “Motion artifacts appear to be tightly related to clinical factors (Fair et al., 2012b) and a whole host of behavioral phenotypes and metrics (Siegel et al., 2016).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Fair et al., 2012b

      Not checked in the free run.

    • cites Siegel et al., 2016

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Strong artifacts due to motion have been noted in diffusion weighted imaging and cortical thickness measurements.

    “Strong artifacts due to motion, in addition to their relevance for fMRI, have been noted in diffusion weighted imaging (Roalf et al., 2016; Yendiki et al., 2014) and cortical thickness measurements (Reuter et al., 2015; Savalia et al., 2017).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Roalf et al., 2016 source

      Not checked in the free run.

    • cites Yendiki et al., 2014 source

      Not checked in the free run.

    • cites Reuter et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Findings of increased subject-to-subject variability in ASD are consistent with different pathologies in brain function leading to related clinical outcomes and underscore the importance of identifying individualized abnormalities.

    “Such findings are consistent with the notion that different pathologies in brain function may lead to related clinical outcomes, and underscore the importance of identifying individualized abnormalities.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Experimental animal models should remain indispensable for probing cellular and molecular markers across the whole human brain.

    “Experimental animal models should therefore remain indispensable for this purpose the foreseeable future.”
    Quote in the paperNot a substantial claim
65 of 65
  • The paper relies on this without support.

    Coordinated activity across distant brain regions is fundamental to human brain function.

    “Coordinated neuronal activity between anatomically disparate regions is an essential feature of human brain function.”
  • The paper relies on this without support.

    The functional connectivity measures used in the reviewed studies reflect neural connectivity rather than non-neural artifacts.

    “A crucial caveat to the above observations is the potential for unidentified sources of artifact in infant studies”
  • The paper relies on this without support.

    Developmental trajectories observed in cross-sectional studies reflect true longitudinal development.

    “Many of the network changes seen during infancy reflect long-term trajectories that extend into childhood and adolescence.”
  • The paper relies on this without support.

    Adult network organization is a valid reference for assessing infant and child network maturity.

    “Indeed, there are now at least 3 reports that suggest the network structure in children as defined by community detection (see Figure 3) are largely similar to the adult (Fair et al., 2012b; Marek et al., 2015; Power et al., 2012).”
  • The paper relies on this without support.

    The studies reviewed are sufficiently comparable to synthesize trends across them.

    “Taken together, these studies point towards several trends that are consistent with results from seed and component based approaches”
  • The paper relies on this without support.

    Microscale architectural features such as gene expression and receptor densities evolve with age.

    “and undoubtedly evolve with age.”
  • The paper relies on this without support.

    Motion tends to be greater in patient populations and younger children.

    “Motion tends to be greater in patient populations and younger children, posing a fundamentally important challenge for developmental research.”
  • The paper relies on this without support.

    Even less is known about the stability of areal parcellations at younger ages.

    “and even less known about the stability of these parcellations at younger ages.”
  • The paper relies on this without support.

    Cortical folding patterns change continually from birth into adulthood, especially during infancy.

    “Cortical folding patterns change continually from birth into adulthood, and especially during infancy.”
  • The paper relies on this without support.

    Infancy is a time during which image contrasts in various MR acquisitions change dramatically.

    “Infancy is also a time during which the image contrasts in various MR acquisitions changes dramatically.”
  • The paper relies on this without support.

    Invasive tract-tracer injections remain the gold standard for identifying and quantifying interareal connection weights.

    “Invasive tract-tracer injections, a method that is only feasible in animal models, remains the “gold standard” for identifying and quantifying interareal connection weights.”
11 of 11

Cites

1 retracted

Flagged first, then by citations

48 of the 259 references couldn’t be matched to a known paper.

Research works printed but not linked: 31

  1. Baker, 2014, Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder, JAMA Psychiatry, 71, 109, 10.1001/jamapsychiatry.2013.3469 · DOI · Paper page
  2. Burgess, 2016, Evaluation of denoising strategies to address motion-correlated artifacts in resting-state functional magnetic resonance imaging data from the human connectome project, Brain Connect, 6, 669, 10.1089/brain.2016.0435 · DOI · Paper page
  3. Calabrese, 2015, A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data, Cereb. Cortex, 25, 4628, 10.1093/cercor/bhv121 · DOI · Paper page
  4. Castellanos, 2016, Intrinsic functional connectivity in attention-deficit/hyperactivity disorder: a science in development, Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 1, 253
  5. Chen, 2016, Distinct global brain dynamics and spatiotemporal organization of the salience network, PLoS Biol., 14, e1002469, 10.1371/journal.pbio.1002469 · DOI · Paper page
  6. Cohen, 2016, The segregation and integration of distinct brain networks and their relationship to cognition, J. Neurosci., 36, 12083, 10.1523/JNEUROSCI.2965-15.2016 · DOI
  7. Collin, 2013, Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex, Cereb. Cortex
  8. Donahue, 2016, Using diffusion tractography to predict cortical connection strength and distance: a quantitative comparison with tracers in the monkey, J. Neurosci., 36, 6758, 10.1523/JNEUROSCI.0493-16.2016 · DOI · Paper page
  9. Eggebrecht, 2017, Joint attention and brain functional connectivity in infants and toddlers, Cereb. Cortex, 10.1093/cercor/bhw403 · DOI · Paper page
  10. Fischl, 2012, FreeSurfer, NeuroImage, 62, 774, 10.1016/j.neuroimage.2012.01.021 · DOI · Paper page
  11. Fuster, 2002, Frontal lobe and cognitive development, J. Neurocytol., 31, 373, 10.1023/A:1024190429920 · DOI · Paper page
  12. Gao, 2013, The synchronization within and interaction between the default and dorsal attention networks in early infancy, Cereb. Cortex, 23, 594, 10.1093/cercor/bhs043 · DOI · Paper page
  13. Gao, 2016, Functional connectivity of the infant human brain: plastic and modifiable, Neuroscientist
  14. Glasser, 2016, The Human Connectome Project's neuroimaging approach, Nat. Neurosci., 19, 1175, 10.1038/nn.4361 · DOI · Paper page
  15. Hindriks, 2016, Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI?, NeuroImage, 127, 242, 10.1016/j.neuroimage.2015.11.055 · DOI · Paper page
  16. Honey, 2009, Predicting human resting-state functional connectivity from structural connectivity, Proc. Natl. Acad. Sci. USA, 106, 2035, 10.1073/pnas.0811168106 · DOI · Paper page
  17. Hwang, 2013, The development of hub architecture in the human functional brain network, Cereb. Cortex, 23, 2380, 10.1093/cercor/bhs227 · DOI · Paper page
  18. Kessler, 2016, Brain oscillations and connectivity in autism spectrum disorders (ASD): new approaches to methodology, measurement and modelling, Neurosci. Biobehav. Rev., 71, 601, 10.1016/j.neubiorev.2016.10.002 · DOI · Paper page
  19. Laumann, 2016, On the stability of BOLD fMRI correlations, Cereb. Cortex, 10.1093/cercor/bhw265 · DOI · Paper page
  20. Lohse, 2014, Resolving anatomical and functional structure in human brain organization: identifying mesoscale organization in weighted network representations, PLoS Comput. Biol., 10, e1003712, 10.1371/journal.pcbi.1003712 · DOI · Paper page
  21. Marquand, 2016, Beyond lumping and splitting: a review of computational approaches for stratifying psychiatric disorders, Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 1, 433
  22. Marusak, 2016, Dynamic functional connectivity of neurocognitive networks in children, Hum. Brain Mapp.
  23. Patriat, 2016, An improved model of motion-related signal changes in fMRI, NeuroImage
  24. Power, 2016, Sources and implications of whole-brain fMRI signals in humans, NeuroImage
  25. Roalf, 2016, The impact of quality assurance assessment on diffusion tensor imaging outcomes in a large-scale population-based cohort, NeuroImage, 125, 903, 10.1016/j.neuroimage.2015.10.068 · DOI · Paper page
  26. Rubinov, 2010, Complex network measures of brain connectivity: uses and interpretations, NeuroImage, 52, 1059, 10.1016/j.neuroimage.2009.10.003 · DOI · Paper page
  27. Savalia, 2017, Motion-related artifacts in structural brain images revealed with independent estimates of in-scanner head motion, Hum. Brain Mapp., 38, 472, 10.1002/hbm.23397 · DOI
  28. Scheinost, 2016, Does prenatal stress alter the developing connectome?, Pediatr. Res.
  29. Siegel, 2016, Data quality influences observed links between functional connectivity and behavior, Cereb. Cortex
  30. Turk, 2016, Cortical chemoarchitecture shapes macroscale effective functional connectivity patterns in macaque cerebral cortex, Hum. Brain Mapp., 37, 1856, 10.1002/hbm.23141 · DOI · Paper page
  31. van den Heuvel, 2016, Multimodal analysis of cortical chemoarchitecture and macroscale fMRI resting-state functional connectivity, Hum. Brain Mapp., 37, 3103, 10.1002/hbm.23229 · DOI

Cited by

Sorted by citations

Authors
Grayson, D. S., & Fair, D. A.
Affiliations
Oregon Health & Science University (US)
Corresponding author
Fair, Damien A.
Venue
NeuroImage
Publisher
Elsevier BV
Published
2017-10
Volume
160
Pages
15-31
ISSN
1053-8119 (ISSN-L)
OpenAlex
W2585998010
Cited by
411
References
259
Citations by year
2026: 35 · 2025: 38 · 2024: 58 · 2023: 45 · 2022: 51 · 2021: 47 · 2020: 49 · 2019: 42 · 2018: 38 · 2017: 8
FWCI
4.19
Type
journal article
Language
en
Open access
Locations
  • NeuroImage (acceptedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Autism Speaks Dennis Weatherstone Predoctoral Fellowship (9591)
  • DeStefano Family Foundation
  • Gates Foundation
  • MacArthur foundation
  • National Institutes of Health (UG3 OD023349, R01 MH105538, R01 MH096773, R01MH107508, P60-AA010760, R01 MH086654, R00MH091238)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords
functional brain networks, developmental trajectories, resting-state functional connectivity, structural connectivity, cognitive development, network science
MeSH terms
Brain, Cognition, Humans, Magnetic Resonance Imaging, Neural Pathways, Neuroimaging

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-09-28.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-09-28.

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