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

“When networks exhibit both high global efficiency and high average clustering coefficients, they exhibit “small-world” organization (Watts and Strogatz, 1998).”

“…to functional connectivity are evolving rapidly Correlated resting-state activity was first identified in bilateral sensorimotor cortex by Biswal et al. (1995), followed soon after by similar findings of bilaterally correlated activity in early visual and early auditory cortex (Cordes et…”

“In animal studies (rodents and non-human primates), this is feasible through the use of comprehensive, histologically and functionally defined whole-brain areal parcellations (Bezgin et al., 2012; Lein et al., 2007; Paxinos et al., 2000; Saleem and Logothetis, 2007; Swanson, 2015; Van Essen et al., 2012).”

“…understood as intrinsic properties of brain function, given that they strongly predict patterns of interregional co-activation across different tasks (Cole et al., 2014; Smith et al., 2009) and are associated with task-relevant behavioral performance (Cole et al., 2012; Lewis et al., 2009).”

“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).”

“There is an abundance of research demonstrating a correlation between DWI-tractography connection weights and FC in adults (Hagmann et al., 2008; Hagmann et al., 2010; Honey et al., 2009).”

“Considerable work and debate is now ongoing to determine the optimal ‘denoising’ approaches during data processing (Patriat et al., 2016; Power et al., 2014).”

“More data-driven approaches were developed based on the concept of independent components analysis (Beckmann and Smith, 2004), which decomposes brain activity into a set of spatial maps (i.”

“Several groups, however, are finding ways to utilize today's non-invasive imaging tools to bring us closer to realizing these goals (Behrens et al., 2003; Glasser et al., 2016a; Gordon et al., 2016; Wig et al., 2014a, 2014b; Zhang et al., 2010).”

“…a well-validated approach to help overcome some of these confounds (Avants et al., 2010; Fonov et al., 2011), and is increasingly adopted in both structural and functional studies of (especially early) development (Eggebrecht et al., 2017; Fonov et al., 2011; Gao et al., 2015a; Scott et al., 2015).”

“…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).”

“…events (e.g. neurogenesis, cell death, myelination, pruning, synaptic plasticity, and glial development) (Innocenti and Price, 2005; Stiles and Jernigan, 2010) and that FC aberrations may point towards the etiological bases of neuropsychiatric disorders (e.g. (Swartz and Monk,…”

“Mounting evidence suggests that the functional connectome exhibits temporal instability that allows it to flexibly switch between multiple different configurations within a scanning session (Allen et al., 2014; Chang and Glover, 2010; Kang et al., 2011; Shen et al., 2015).”

“The cerebral cortex is both anatomically and functionally organized at many physical scales - starting at the level of single neurons and extending up to functional systems (Churchland and Sejnowski, 1992).”

“The authors contend that these changes potentially support the ability to traverse through more diverse cognitive states in order to accomplish increasingly complex task demands (Bassett et al., 2011; Braun et al., 2015).”

“Similar to the participation coefficient of a given node, one can compute the network's global integrative capacity by taking into account the network modules and the interdependencies between them (de Reus and van den Heuvel, 2014; Tononi et al., 1994).”

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

“…expression (Richiardi et al., 2015), and synaptic receptor densities (Turk et al., 2016; van den Heuvel et al., 2016b) – properties that, in turn, undergo experience-dependent and activity-dependent modulation over the lifespan (Huttenlocher, 2002; Markham and Greenough, 2004; Scholz et al., 2009).”

“Functional network analyses that strongly relate to known network organization may therefore find signal homogeneity within parcels to be a useful optimization criterion for choosing a parcellation (e.g. see Gordon et al. (2016) and Glasser et al. (2016a)).”

“In particular, it has been revealed that motion increases non-specific local coupling and decreases long-range coupling in ways that are similar to differences found between children and adults (Fair et al., 2012b; Power et al., 2012; Satterthwaite et al., 2012; Yan et al., 2013).”

“(1995), 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).”

“…areas (and indeed, connectivity within other cognitive RSNs) continues to strengthen from early childhood throughout development, especially with respect to long-range anterior-posterior links (de Bie et al., 2012; Fair et al., 2008; Sato et al., 2014; Sherman et al., 2014; Supekar et al., 2010).”

“Returning to the MRI literature, there is convergent evidence that the locations of high-strength and high-betweenness hub regions appear to be stable after 5 years of age (Cao et al., 2014; Grayson et al., 2014; Hwang et al., 2013; Wang et al., 2012; Wu et al., 2013; Zuo et al., 2012).”

“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).”

“2A), 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).”

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

“2A), 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).”

“Moving forward, there is strong consensus about the importance of preventing head motion during acquisition and rigorously quantifying motion effects in study data (Goto et al., 2016; Power et al., 2015; Siegel et al., 2016).”

“Cutting-edge work in resting-state fMRI acquisition and network analysis suggests that individual brains, even among typical subjects, are distinguishable via their functional connectomes (Finn et al., 2015; Laumann et al., 2015; Miranda-Dominguez et al., 2014b).”

“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.”

“…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).”

“The authors contend that these changes potentially support the ability to traverse through more diverse cognitive states in order to accomplish increasingly complex task demands (Bassett et al., 2011; Braun et al., 2015).”

“…componentbased approaches demonstrate the existence of robust, bilateral segregated networks for somatomotor, primary auditory, primary visual, and extrastriate visual cortex (Fransson et al., 2007; Gao et al., 2015a; Kiviniemi et al., 2000; Lin et al., 2008; Liu et al., 2008; Smyser et al., 2010).”

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

“The network's behavior can thus be modeled as a set of properties that emerge from the network's unique global structure and local features (Sporns, 2014).”

“Multiple studies have found evidence for limited test-retest reliability using a multitude of conventional rs-fcMRI network characteristics and analytic approaches (Braun et al., 2012; Wang et al., 2011; Wisner et al., 2013; Zuo et al., 2010; Zuo and Xing, 2014).”

“On top of these issues, functional areal boundaries (see Parcellation Choice) of heteromodal association areas are variable with respect to sulcal and gyral anatomy (Fischl et al., 2008).”

“Unfortunately, follow-up work on this topic in humans has been relatively scant, and this work was prior to new information regarding tractography artifacts (Calabrese et al., 2015; Donahue et al., 2016; Reveley et al., 2015; Thomas et al., 2014), and prior to systematic motion artifacts being demonstrated in diffusio…”

“There is an abundance of research demonstrating a correlation between DWI-tractography connection weights and FC in adults (Hagmann et al., 2008; Hagmann et al., 2010; Honey et al., 2009).”

“…componentbased approaches demonstrate the existence of robust, bilateral segregated networks for somatomotor, primary auditory, primary visual, and extrastriate visual cortex (Fransson et al., 2007; Gao et al., 2015a; Kiviniemi et al., 2000; Lin et al., 2008; Liu et al., 2008; Smyser et al., 2010).”

“…global functional network topology in conscious versus unconscious state in adults (Spoormaker et al., 2010), but key differences have been found in corticocortical (Heine et al., 2012; Horovitz et al., 2009; Spoormaker et al., 2010) and thalamocortical (Spoormaker et al., 2010) connectivity.”

“Multiple studies have found evidence for limited test-retest reliability using a multitude of conventional rs-fcMRI network characteristics and analytic approaches (Braun et al., 2012; Wang et al., 2011; Wisner et al., 2013; Zuo et al., 2010; Zuo and Xing, 2014).”

“These areal boundaries appear very early in development (Kostovic et al., 1995) and each area is thought to make a distinct contribution to information processing (Cohen et al., 2008; Felleman and Van Essen, 1991; Fuster, 2002; O'Leary and Nakagawa, 2002; Sur and Rubenstein, 2005).”

“DSG was supported by an Autism Speaks Dennis Weatherstone Predoctoral Fellowship (#9591).”

“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).”

“…age-specific and study-specific template brain images for image registration is a well-validated approach to help overcome some of these confounds (Avants et al., 2010; Fonov et al., 2011), and is increasingly adopted in both structural and functional studies of (especially early) development…”

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

“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).”

“Greater global efficiency in structural and functional networks has been linked to higher IQ, attentional capacity, and working memory in healthy young adults (Cohen and D'Esposito, 2016; Kitzbichler et al., 2011; Li et al., 2009; Stanley et al., 2015; van den Heuvel et al., 2009), supporting the notion that it confer…”

“These areal boundaries appear very early in development (Kostovic et al., 1995) and each area is thought to make a distinct contribution to information processing (Cohen et al., 2008; Felleman and Van Essen, 1991; Fuster, 2002; O'Leary and Nakagawa, 2002; Sur and Rubenstein, 2005).”

“…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).”

“, 2015), or sparser analytic predictions of FC using graph metrics of mutual communication (Goni et al., 2014; Grayson et al., 2016) (although, both approaches appear to be comparably effective; see Fig.”

“As an example, simulation experiments using structure-function models have predicted that even purely focal and transient perturbations in activity should result in diffuse network reorganization that affects distant brain systems (Alstott et al., 2009; Honey and Sporns, 2008; Misic et al., 2015).”

“…areas (and indeed, connectivity within other cognitive RSNs) continues to strengthen from early childhood throughout development, especially with respect to long-range anterior-posterior links (de Bie et al., 2012; Fair et al., 2008; Sato et al., 2014; Sherman et al., 2014; Supekar et al., 2010).”

“…and betweenness hubs in adulthood are largely located within the default mode, attentional, sensorimotor, and visual areas (Cao et al., 2014; Fransson et al., 2011; Grayson et al., 2014; Hwang et al., 2013), whereas neonatal hubs primarily involve early sensorimotor, visual, and limbic…”

“DSG was supported by an Autism Speaks Dennis Weatherstone Predoctoral Fellowship (#9591).”

“Models can involve highly parameterized simulations of regional activity (Hansen et al., 2015; Messe et al., 2014; Sanz-Leon et al., 2015), or sparser analytic predictions of FC using graph metrics of mutual communication (Goni et al., 2014; Grayson et al., 2016) (although, both approaches appear…”

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

“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).”

“There is ongoing debate regarding the adequacy of these techniques (Jo et al., 2010; Power et al., 2016), and more work may be warranted to determine optimal ways to account for age-related physiological confounds.”

“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.”

“By far, strength and betweenness have been the most popular hub metrics within neuroimaging, although others such as eigenvector centrality (Lohmann et al., 2010; Zuo et al., 2012) and node communicability (de Reus and van den Heuvel, 2014; Mantzaris et al., 2013) have seen useful application as…”

“…consistently implicated in Schizophrenia (Baker et al., 2014; Khadka et al., 2013; Satterthwaite et al., 2015), ADHD (Castellanos and Aoki, 2016; Fair et al., 2012b), and Autism (Kessler et al., 2016; Moseley et al., 2015; Supekar et al., 2013) – though a thorough examination of this literature…”

“The network's behavior can thus be modeled as a set of properties that emerge from the network's unique global structure and local features (Sporns, 2014).”

“…consistently implicated in Schizophrenia (Baker et al., 2014; Khadka et al., 2013; Satterthwaite et al., 2015), ADHD (Castellanos and Aoki, 2016; Fair et al., 2012b), and Autism (Kessler et al., 2016; Moseley et al., 2015; Supekar et al., 2013) – though a thorough examination of this literature…”

“, 2014) and cortical thickness measurements (Reuter et al., 2015; Savalia et al., 2017).”

“…expression (Richiardi et al., 2015), and synaptic receptor densities (Turk et al., 2016; van den Heuvel et al., 2016b) – properties that, in turn, undergo experience-dependent and activity-dependent modulation over the lifespan (Huttenlocher, 2002; Markham and Greenough, 2004; Scholz et al., 2009).”

“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).”

“…and functional networks has been linked to higher IQ, attentional capacity, and working memory in healthy young adults (Cohen and D'Esposito, 2016; Kitzbichler et al., 2011; Li et al., 2009; Stanley et al., 2015; van den Heuvel et al., 2009), supporting the notion that it confers advantages for…”

“Multiple studies have found evidence for limited test-retest reliability using a multitude of conventional rs-fcMRI network characteristics and analytic approaches (Braun et al., 2012; Wang et al., 2011; Wisner et al., 2013; Zuo et al., 2010; Zuo and Xing, 2014).”

“There is currently no consensus regarding an optimal set of criteria for defining an areal parcellation (Craddock et al., 2013; Glasser et al., 2016a; Gordon et al., 2016), and even less known about the stability of these parcellations at younger ages.”

“For example, structure-function modeling using MRI data suffers from a number of inherent limitations in DWI-tractography that have not been overcome by state-of-the-art acquisition and processing approaches (Calabrese et al., 2015; Donahue et al., 2016; Reveley et al., 2015; Thomas et al., 2014).”

“Indeed, recent work suggests that Autism Spectrum Disorder is characterized by increased subject-to-subject variability relative to the general population (Hahamy et al., 2015).”

“Multiple studies have found evidence for limited test-retest reliability using a multitude of conventional rs-fcMRI network characteristics and analytic approaches (Braun et al., 2012; Wang et al., 2011; Wisner et al., 2013; Zuo et al., 2010; Zuo and Xing, 2014).”

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

“There is also a progressive shift in peak amplitude towards higher frequency activity (Miskovic et al., 2015; Rodriguez-Martinez et al., 2015; Smit et al., 2012; Whitford et al., 2007).”

“In neonates, two independent rs-fcMRI studies found evidence for modules comprised largely of anatomically proximate areas (De Asis-Cruz et al., 2015; van den Heuvel et al., 2015b).”

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

“…componentbased approaches demonstrate the existence of robust, bilateral segregated networks for somatomotor, primary auditory, primary visual, and extrastriate visual cortex (Fransson et al., 2007; Gao et al., 2015a; Kiviniemi et al., 2000; Lin et al., 2008; Liu et al., 2008; Smyser et al., 2010).”

“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).”

“These findings suggest that the development of a small-world architecture, as well as the capacity for globally efficient communication and integration, largely occurs during the first year of life and prenatally, a finding that is supported by multimodal structural and functional network analysis in preterm infants (…”

“Given that macroscale FC is modulated by both interregional connectivity strength as well as local population dynamics (Sanz-Leon et al., 2015), alterations in SC-FC coupling could potentially point to important shifts in the underlying drivers of various network phenomena.”

“…componentbased approaches demonstrate the existence of robust, bilateral segregated networks for somatomotor, primary auditory, primary visual, and extrastriate visual cortex (Fransson et al., 2007; Gao et al., 2015a; Kiviniemi et al., 2000; Lin et al., 2008; Liu et al., 2008; Smyser et al., 2010).”

“These data agree with notions that temporal variability in very low frequency correlations is an emergent, hidden property of higher frequency power spectra (Chang et al., 2013; Tagliazucchi et al., 2012), which is known to change continuously throughout development (Miskovic et al.”

“As an example, simulation experiments using structure-function models have predicted that even purely focal and transient perturbations in activity should result in diffuse network reorganization that affects distant brain systems (Alstott et al., 2009; Honey and Sporns, 2008; Misic et al., 2015).”

“Several groups, however, are finding ways to utilize today's non-invasive imaging tools to bring us closer to realizing these goals (Behrens et al., 2003; Glasser et al., 2016a; Gordon et al., 2016; Wig et al., 2014a, 2014b; Zhang et al., 2010).”

“Even the best-performing SC-FC models generally account for less than 50% of the variance in FC across the brain in both humans and non-human primates (Grayson et al., 2016; Messe et al., 2014; Misic et al., 2015).”

“Despite this “adult like” level of organization, refinements within and between systems do 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).”

“At finer resolutions, several other modules can be identified (Doucet et al., 2011; Gordon et al., 2016; Power et al., 2011; Yeo et al., 2011), including hierarchical visual subdivisions, topographical somatomotor subdivisions, an auditory module, a limbic module, a ventral attention module, and other smaller subdivis…”

“These data agree with notions that temporal variability in very low frequency correlations is an emergent, hidden property of higher frequency power spectra (Chang et al., 2013; Tagliazucchi et al., 2012), which is known to change continuously throughout development (Miskovic et al.”

“These areal boundaries appear very early in development (Kostovic et al., 1995) and each area is thought to make a distinct contribution to information processing (Cohen et al., 2008; Felleman and Van Essen, 1991; Fuster, 2002; O'Leary and Nakagawa, 2002; Sur and Rubenstein, 2005).”

“, 2010) and thalamocortical (Spoormaker et al., 2010) connectivity.”

“These coincident trajectories have provided key support for the hypothesis that developmental changes in baseline electrophysiological signatures may primarily be subserved by reduction of neuropil and progressive synapse elimination (Buchmann et al., 2011; Smit et al., 2012; Whitford et al., 2007).”

“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).”

“…global functional network topology in conscious versus unconscious state in adults (Spoormaker et al., 2010), but key differences have been found in corticocortical (Heine et al., 2012; Horovitz et al., 2009; Spoormaker et al., 2010) and thalamocortical (Spoormaker et al., 2010) connectivity.”

“Future work could probably improve these relationships substantially by imposing rigorous anatomical constraints in the tractography process (Smith et al., 2015), but such efforts have not seen extensive validation yet.”

“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…”

“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.”

“5) are attainable across species (Grayson et al., 2016; Miranda-Dominguez et al., 2014b; Stafford et al., 2014; Hutchison et al., 2015; Hutchison and Everling, 2012; Margulies et al., 2009).”