Functional connectivity in the developing brain: a longitudinal study from 4 to 9months of age

“05 (Benjamini and Hochberg, 1995) are enclosed with black squares.”

“The despiking process involved detecting outliers as implemented in AFNI's 3dDespike and then replacing detected outliers with values from a third order spline fit to the clean portions of neighboring data.”

“Finally this group reduced matrix was decomposed into 30 or 100 spatially independent components using the Infomax ICA algorithm (Bell and Sejnowski, 1995) for low and high model order decompositions respectively.”

“5 in Power et al., 2012).”

“5, some ICNs appeared to have merged to form a single network as seen in an adult ICN decomposition (here we compare to Smith et al., 2009).”

“Similar model orders have been used by a number of labs (Allen et al., 2012; Damoiseaux et al., 2006; Filippini et al., 2009).”

“Spatial GICA linearly decomposes data into temporally-coherent maximally independent spatial source signals (Calhoun et al., 2001).”

“Recent studies have demonstrated non-stationarity in fMRI time courses (Chang and Glover, 2010; Jones et al., 2012; Sakoglu et al., 2010); therefore future work should consider probing the changes in the dynamics of ICNs (Allen et al., 2012; Cribben et al., 2012).”

“…work identifying ICNs in infants (Fransson et al., 2007) and numerous subsequent studies of resting state connectivity have provided greater understanding of the functional architecture of the human brain during early development (Doria et al., 2010; Dosenbach et al., 2010; Gao et al., 2009).”

“Recent studies have demonstrated non-stationarity in fMRI time courses (Chang and Glover, 2010; Jones et al., 2012; Sakoglu et al., 2010); therefore future work should consider probing the changes in the dynamics of ICNs (Allen et al.”

“Furthermore ICNs are shown to be present under the conditions of mild anesthesia (Greicius et al., 2008; Vincent et al., 2007) as well as sleep (Larson-Prior et al.”

“Similar model orders have been used by a number of labs (Allen et al., 2012; Damoiseaux et al., 2006; Filippini et al., 2009).”

“It has been suggested that functional brain networks develop in a local to distributed fashion (Fair et al., 2009), and indeed the increased coherencewe found between The quality index (Iq) associated with each ICN is listed in parentheses adjacent to the component number.”

“…2000) and is related to a child's early social development and attachment, as is commonly noted when a typically developing 6 to 9 month old child screams when a stranger walks into the room, or when mother walks out of sight (Hay et al., 2012), for review see Whitfield-Gabrieli and Ford (2012).”

“…measures have recommended using a subject motion summary measure such as mean framewise displacement (meanFD) as a subject level nuisance covariate during group-level statistical comparisons to mitigate motion effects on connectivity measures (Satterthwaite et al., 2012; Yan et al., 2013).”

“Such imaging studies are consistent with previous post-mortem investigations identifying cellular processes in early childhood such as dendritic maturation, fluctuating synaptic density, and myelination that vary depending on brain region and age (Glantz et al., 2007; Huttenlocher and Dabholkar, 1997; Petanjek et al.,…”

“…changes in cortical thickness and volume that vary throughout the brain (Giedd and Rapoport, 2010) and may be sensitive to disorders such as prematurity (Phillips et al., 2011), autism (Castelli et al., 2002; McAlonan et al., 2005) or other developmental disabilities (Seidman et al., 2005).”

“Damaraju et al. / NeuroImage 84 (2014) 169–180”

“The stability of the ICA decomposition was estimated by calculating a cluster quality index for each component cluster, which ranges between 0 and 1 (Himberg et al., 2004).”

“The majority of previous work characterizes children over 3 years of age (for review see Giedd and Rapoport, 2010), although recent reports include children in the first several years of life — when a dramatic increase in volume occurs (Gilmore et al., 2011; Knickmeyer et al., 2008).”

“Time courses of retained ICNs were used to compute 1) power spectra and2) functional network connectivity (FNC), defined as the pairwise correlation between ICA time courses (Jafri et al., 2008).”

“Here, we follow their recommendation and use a model order of 30, the average Minimum Description Length (MDL) for single subject datasets (Li et al., 2007), and a high model order of 100, the upper limit recommendedbyAbou-Elseoud et al. (2010) beyond which network stability was found to decrease.”

“Recent high-resolution MRI studies identify age-dependent changes in cortical thickness and volume that vary throughout the brain (Giedd and Rapoport, 2010) and may be sensitive to disorders such as prematurity (Phillips et al., 2011), autism (Castelli et al., 2002; McAlonan et al., 2005) or other…”

“Smyser et al. (2010) used seed-based correlational analysis in neonates beginning at 26 week gestation, identifying neural networks which increase in distance and coherence through gestation.”

“…becomes more efficient and thus requires fewer neuronal circuits, which is consistentwith post-mortem studies at this age demonstrating synaptic pruning and cortical thinning as part of normal development (Huttenlocher and Dabholkar, 1997; Huttenlocher et al., 1982; Shankle et al., 1999).”

“Components of the default mode network putatively support self reflection (Whitfield-Gabrieli et al., 2011) and social cognition (Saxe et al., 2004), with the posterior cingulate cortex particularly important for emotional processing of faces (Ramasubbu et al., 2007).”

“Subject-specific ICA spatial maps and corresponding time courses were computed by back-reconstruction using spatio-temporal or dual regression (Erhardt et al., 2011).”

“Fransson et al. published the initial work identifying ICNs in infants (Fransson et al., 2007) and numerous subsequent studies of resting state connectivity have provided greater understanding of the functional architecture of the human brain during early development (Doria et al., 2010; Dosenbach…”

“…changes in cortical thickness and volume that vary throughout the brain (Giedd and Rapoport, 2010) and may be sensitive to disorders such as prematurity (Phillips et al., 2011), autism (Castelli et al., 2002; McAlonan et al., 2005) or other developmental disabilities (Seidman et al., 2005).”

“Recent studies have demonstrated non-stationarity in fMRI time courses (Chang and Glover, 2010; Jones et al., 2012; Sakoglu et al., 2010); therefore future work should consider probing the changes in the dynamics of ICNs (Allen et al., 2012; Cribben et al., 2012).”

“Using ICA to identify regions associatedwith the adult defaultmode network, therewas evidence for a rudimentary default mode network consisting of 6 regions in the infants that expanded to 13 regions at 1 year of age and 19 regions at 2 years (Gao et al., 2009).”

“Consistentwith a prior report (Doria et al., 2010), it is possible that these primary sensory networks are present from birth.”

“Intrinsic connectivity networks (ICNs) observed during resting state fMRI (rsfMRI) have shown close correspondence to networks observed across several tasks (Calhoun et al., 2008; Filippini et al., 2009) thereby providing an objective way to probe network organization without task confounds.”

“Furthermore ICNs are shown to be present under the conditions of mild anesthesia (Greicius et al., 2008; Vincent et al., 2007) as well as sleep (Larson-Prior et al.”

“…changes in cortical thickness and volume that vary throughout the brain (Giedd and Rapoport, 2010) and may be sensitive to disorders such as prematurity (Phillips et al., 2011), autism (Castelli et al., 2002; McAlonan et al., 2005) or other developmental disabilities (Seidman et al., 2005).”

“This approach has been used to better characterize clinical disorders of abnormal brain network development such as schizophrenia (Filippini et al., 2009), autism (Di Martino et al., 2011; Jones et al., 2010) and attention deficit hyperactivity disorder (Mennes et al., 2011).”

“, 2007) as well as sleep (Larson-Prior et al., 2009).”

“Recent studies have demonstrated non-stationarity in fMRI time courses (Chang and Glover, 2010; Jones et al., 2012; Sakoglu et al., 2010); therefore future work should consider probing the changes in the dynamics of ICNs (Allen et al., 2012; Cribben et al., 2012).”

“Components of the default mode network putatively support self reflection (Whitfield-Gabrieli et al., 2011) and social cognition (Saxe et al.”

“This approach has been used to study ICNs in adults (Kiviniemi et al., 2009) but it has not previously been applied to children.”

“A clear advantage of the higher order ICA decomposition was that it divided relatively large spatial networks into smaller sub-networks such that we could study the functional connectivity between them (Abou-Elseoud et al., 2010).”

“Recent studies have demonstrated non-stationarity in fMRI time courses (Chang and Glover, 2010; Jones et al., 2012; Sakoglu et al., 2010); therefore future work should consider probing the changes in the dynamics of ICNs (Allen et al., 2012; Cribben et al., 2012).”

“…post-mortem investigations identifying cellular processes in early childhood such as dendritic maturation, fluctuating synaptic density, and myelination that vary depending on brain region and age (Glantz et al., 2007; Huttenlocher and Dabholkar, 1997; Petanjek et al., 2011; Webster et al., 2011).”

“The technology needed for optimal data acquisition and processing methods for infant studies, and the factors involved in the interpretation of cerebral development in infants on the basis of intrinsic networks obtained from fcMRI, has been recently reviewed (Smyser et al., 2011).”

“Using children from this same cross sectional dataset, Lin et al. (2008) showed that the sensorimotor cortex had functional connectivity with larger areas of the brain than the visual cortex did at 1 year of age, but by 2 years both areas were similar.”

“A slightly higher upper frequency cut off of 0.15 Hzwas chosen instead of typical 0.08 or 0.1 Hz for the bandpassfiltering as some recent studies have demonstrated the broadband nature of neuronal signals underlying BOLD time courses (Niazy et al., 2011).”

“This approach has been used to better characterize clinical disorders of abnormal brain network development such as schizophrenia (Filippini et al., 2009), autism (Di Martino et al., 2011; Jones et al., 2010) and attention deficit hyperactivity disorder (Mennes et al., 2011).”

“The common template was the 9 month template in the MNI stereotaxic standard space as provided by Cincinnati children's research hospital (Altaye et al., 2008).”

“Additionally as more common group variance is captured at highmodel order ICA, the ICA algorithmwill be able to separate cleaner sources thereby increasing the ability to detect differences between groups (Abou-Elseoud et al., 2011).”

“…based analysis of children at 12 months of age, Liu evaluated functional connectivity with the sensorimotor cortex and found greater intrahemispheric than interhemispheric connectivity, suggesting that cross-callosal connectivity develops later than within-hemisphere networks (Liu et al., 2008).”

“This approach has been used to better characterize clinical disorders of abnormal brain network development such as schizophrenia (Filippini et al., 2009), autism (Di Martino et al., 2011; Jones et al., 2010) and attention deficit hyperactivity disorder (Mennes et al., 2011).”

“…becomes more efficient and thus requires fewer neuronal circuits, which is consistentwith post-mortem studies at this age demonstrating synaptic pruning and cortical thinning as part of normal development (Huttenlocher and Dabholkar, 1997; Huttenlocher et al., 1982; Shankle et al., 1999).”

“Such imaging studies are consistent with previous post-mortem investigations identifying cellular processes in early childhood such as dendritic maturation, fluctuating synaptic density, and myelination that vary depending on brain region and age (Glantz et al., 2007; Huttenlocher and Dabholkar, 1997; Petanjek et al.,…”

“Recent high-resolution MRI studies identify age-dependent changes in cortical thickness and volume that vary throughout the brain (Giedd and Rapoport, 2010) and may be sensitive to disorders such as prematurity (Phillips et al., 2011), autism (Castelli et al.”

“Accounting for more variance at the subject level data reduction improves the estimation of group aggregate spatial maps as well as back reconstructed subjectspecific maps and time-courses (Erhardt et al., 2011; Esposito and Goebel, 2011).”

“, 2004), with the posterior cingulate cortex particularly important for emotional processing of faces (Ramasubbu et al., 2007).”

“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).”

“Consistently, Damaraju et al. (2013) imaged normal pediatric subjects at 4 and 9 months and showed decreased local functional connectivity and increased distant connectivity, exemplifying the dynamic functional maturation process during this critical period.”

“We expected some connectivity measures to be better captured in a static model and others in a dynamic model (Damaraju et al., 2014).”

“By 4 years of age, there is marked increase in connectivity and the DMN becomes similar to what is observed in adults (Damaraju et al., 2014; Gao et al., 2009; Lee et al., 2013).”

“However, the long-range connections, which were less developed during the prenatal period, primarily appear in 1-year-olds and strengthen in 2-year-olds, making the brain networks more globally integrated [9,10,24,25].”

“Between 4 and 9 months of age, a similar network localization is observed but the connectivity strength decreases in local networks and increases in more distant networks.(191) Regarding higher-order cognitive processes, an immature default mode network (“protoDMN”) is usually found in newborns, whereas integrated net…”

“We defined 71 functional nodes in our population, this is in line with previous studies in developmental populations (Damaraju et al., 2014) and offered good cerebral coverage coupled with anatomically distinct nodes (Fig.”

“…two postnatal years local connectivity decreases and global connectivity via long-range functional connections increases in a process especially characterized by a complex reorganization of the hubs (Damaraju et al., 2014; Fan et al., 2011; Gao et al., 2016; Hagmann et al., 2010; Yap et al., 2011).”

“(rs-fMRI) has been emerging for probing functional brain development (Gao et al., 2009; Smyser et al., 2010; Fransson et al., 2011; Gao et al., 2011; Smyser et al., 2011; Barrett and Satpute, 2013; Alcauter et al., 2014; Damaraju et al., 2014; De Asis-Cruz et al., 2015; Gao et al., 2015a; Gao et al., 2015b; Van den He…”

“State); one state represented high synchrony for regions mainly in the sensorimotor cortex (SM State); and one state comprised high levels of synchronisation in the frontal cortex, angular gyrus, and posterior cingulate gyrus (for simplicity we refer to this as frontoparietal or FP state).”

“A study focused on development from four to ninemonths found that the strength of connectivity decreased in all ICA-identified networks except the default mode, including in the auditory and temporal networks (Damaraju et al., 2014).”

“Some investigators have reported increasing long- /decreasing short-range functional connectivity, with increased default mode network connectivity between four and nine months (Damaraju et al., 2013).”

“With the development of the brain, functional connectivity undergoes substantial changes, which demonstrate the strengthening and pruning of brain connectivity between different cortical regions (Damaraju et al., 2014; Cao et al., 2017b).”

“These results thus need to be replicated both for the current age range and other developmental stages, as studied for other neural systems (Antonenko et al., 2013; Bernard et al., 2013; Damaraju et al., 2014; Gabard-Durnam et al., 2014).”

“One such region that may be uniquely important early in development is the posterior hub of the default mode network (Damaraju et al., 2014; Gao et al., 2009, 2013; Pruett et al., 2015).”

“Hence, most fMRI studies with infants have been done with them sleeping [74,75] or sedated [76,77].”

“This increasing efficiency is paralleled by decreasing segregation as result of synaptic pruning and the refinement of the specialized sub-networks (Damaraju et al. , 2014).”

“…2014; Righi et al., 2014; T oth et al., 2017), while most of the studies using fMRI have focused on resting-state connectivity in sleeping infants (Damaraju et al., 2014; Emberson et al., 2015; Fransson et al., 2011; Gao et al., 2016; Kwon et al., 2016; Lin et al., 2008; Lu et al., 2010; Marrus…”

“…most of these studies utilize functional connectivity MRI (fcMRI) to identify RSNs (Fransson et al., 2007; Doria et al., 2010; Smyser et al., 2010; Damaraju et al., 2014), functional near-infrared spectroscopy (fNIRS) has emerged as a promising modality due to its practical advantages, which…”

“These sensory and association networks undergo subtle refinements and strengthening over the first two years of life and by age two bear substantial resemblance to their adult counterparts (Alcauter et al. 2015; Damaraju et al. 2014; Gao et al. 2015a,b; Graham et al. 2015).”

“18,28,81,83 Due to the marked spatial symmetry observed in components FCC 3 to FCC 8, we presented them in pairs in Fig.”

“Although 30 components are more frequently used, 100 component ICA is increasingly common (Damaraju et al., 2014; Wu et al., 2015).”

“At this stage, the DMN is still in the process of rapid development (Damaraju et al., 2014; Gao et al., 2016).”

“Damaraju et al. (2014) recently characterized the development of intrinsic connectivity networks (ICNs) in infants aged between 4 and 9 months with resting state MRI (rsMRI) performed while sleeping without sedative medication.”

“Nostatisticalmethodswereusedtopre-determinesamplesize,butour samplesizeislargerthanwhathasbeenreportedinpreviouspublications evaluatingresting-stateconnectivityinearlyinfancy 44 – 46 .”

“In typically developing infants, functional integration and segregation of brain networks undergo maturation during the first year of life, generally manifested as increasing connectivity in functionally-relevant regions (Damaraju et al., 2014; Huang et al., 2015).”

“These findings are somewhat consistent with those of a study of 4-to 9-month-old children (Damaraju et al., 2014).”

“increase during early brain development but at a different pace or slope.(67) For a better visualization of the fto-FC in our study, we plotted the stimulus-evoked time course of changes in Δ1⁄2O2Hb , Δ1⁄2tHb , and Δ1⁄2HHb at the left FTL with respect to those at the VC (Fig.”

“…in both short-range connectivity between anatomically proximal regions and long-range global connections between anatomically distant regions ( Damaraju et al., 2014; Fransson et al., 2007; Gao et al., 2009; Moore et al., 2023; Smyser et al., 2010; Sylvester et al., 2022; Wylie et al., 2014).”

“, frontal to visual and frontal to sensorimotor regions), with the exception of the posterior cingulate cortex which maintains a high level of intra-network connectivity profile (Damaraju et al., 2014).”

“Existing longitudinal studies have applied cross-sectional approaches to identify subject-specific IFNs; that is, IFNs are esti- mated independently for rs-fMRI of each visit (Damaraju et al., 2014; Gao, Alcauter, Smith, Gilmore, & Lin, 2015; Odish et al., 2015; van der Horn et al., 2017).”

“In these studies, the term ‘state’ refers to whole-brain stable FC configurations recurring across participants and time (Allen et al., 2014; Damaraju et al., 2014; Gonzalez-Castillo et al., 2015; Valsasina et al., 2019).”

“A. Fiske et al. Whilst previous longitudinal research has examined resting state functional connectivity development in infancy (Damaraju et al., 2014), as well as the functional activation underpinning working memory in infancy (Reyes et al., 2020) and cognitive flexibility in early childhood…”

“Scan times were not reported in 38% of articles with success rates ranging from 43–100% x = 87.4% (Bartha et al., 2007; Damaraju et al., 2014; Golan et al., 2011; Groves et al., 2012; Inder et al., 2005; Knickmeyer et al., 2008; Lin et al., 2008; Maas et al., 2004; McNally et al., 1997; Miller et…”

“Similarly, Damaraju et al. found increasing coherence within the posterior DMN between 4 and 9 months, and noted that executive and frontoparietal networks showed more prolonged maturation 66 .”

“Over the past two decades, MRI has been increasingly used in neonates and infants to elucidate patterns of brain development (Damaraju et al., 2014; Kline et al., 2021; Zhang et al., 2021) and to quickly and accurately diagnose suspected intraparenchymal pathologies, such as ischemia and hemorrhage (Reddy, 2022).”

“In addition, functional network segregation and integration proceed from childhood to adulthood, which is characterized by an increase in distant networks and a decrease in local networks (Fair et al., 2009; Vogel et al., 2010; Damaraju et al., 2014).”

“Additionally, we observed long-range right frontal-posterior FC increased with age and exhibited positive correlations at 24 months, as consistent with previous infant studies (29, 31).”

“In addition, we expected some connectivity measures to be better captured in a static model and others in a dynamic model [12].”

“…connectivity develops first, followed by the enhancement of long-range functional connectivity and its continued maturation throughout childhood (Cao et al., 2017a; Damaraju et al., 2014b; Fair et al., 2009; Jakab et al., 2014; Smyser et al., 2010; Thomason et al., 2014; Thomason et al., 2015).”

“In particular, while there was evidence for the expected increase in long-range connectivity, there was no expected decrease in short-range connectivity (Damaraju et al., 2014).”

“Prior infant studies have identified several ICNs 7–9, 11, 12, 32– 34 , yet only a subset Our findings offer critical insights into neurodevelopment, particularly the early formation of brain network architecture.”

“12 Even across this smaller age range (2 months), changes were apparent in these 2 networks.”

“Also, connections between areas mature with time: for example, at 9 months the connections over longer distance are emerging, while local network connectivity decreases (Damaraju et al., 2014).”

“…from infancy to adulthood is not yet well known, functional connectivity measures in infancy show increased complexity and e ffi ciency (Boersma et al., 2011; Cao et al., 2016; Damaraju et al., 2014) and a significant reorganisation in adolescence (Gabard-Durnam et al., 2014; Uhlhaas et al., 2009).”

“78 Fourth, motion during scanning was a signi fi cant covariate in our analyses, and although we adjusted for it statistically, its in fl uence represents a potential limitation.”

“However, it remains inconsistent that the FNC increases (Gao et al., 2015) or decreases (Damaraju et al., 2014; Zhang et al., 2017) with age during early brain development in previous reports.”

“…networks emerge from localized patterns of connectivity that gradually integrate into distributed systems supporting flexible cognition (Fransson et al., 2007; Gao et al., 2009; Smyser et al., 2010; Damaraju et al., 2014; Wylie et al., 2014; De Asis-Cruz et al., 2015; Van Den Heuvel et al., 2015).”

“Additionally, we observed long-range right frontal-posterior FC increased with age and exhibited positive correlations at 24 months, as consistent with previous infant studies ( Damaraju et al., 2014 ; Bulgarelli et al., 2020b ).”