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Cited by 115Functional Brain Connectivity StudiesNeural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on Behavior

A three-wave longitudinal study of subcortical–cortical resting-state connectivity in adolescence: Testing age- and puberty-related changes

Open access
van Duijvenvoorde, Anna C. K., Westhoff, Bianca, de Vos, Frank, Wierenga, Lara M., Crone, Eveline A.·2019·Human Brain Mapping
DOI 10.1002/hbm.24630PMC PMC6767490
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Abstract

Adolescence is the transitional period between childhood and adulthood, characterized by substantial changes in reward‐driven behavior. Although reward‐driven behavior is supported by subcortical‐medial prefrontal cortex (PFC) connectivity, the development of these circuits is not well understood. Particularly, while puberty has been hypothesized to accelerate organization and activation of functional neural circuits, the relationship between age, sex, pubertal change, and functional connectivity has hardly been studied. Here, we present an analysis of resting‐state functional connectivity between subcortical structures and the medial PFC, in 661 scans of 273 participants between 8 and 29 years, using a three‐wave longitudinal design. Generalized additive mixed model procedures were used to assess the effects of age, sex, and self‐reported pubertal status on connectivity between subcortical structures (nucleus accumbens, caudate, putamen, hippocampus, and amygdala) and cortical medial structures (dorsal anterior cingulate, ventral anterior cingulate, subcallosal cortex, frontal medial cortex). We observed an age‐related strengthening of subcortico‐subcortical and cortico‐cortical connectivity. Subcortical–cortical connectivity, such as, between the nucleus accumbens—frontal medial cortex, and the caudate—dorsal anterior cingulate cortex, however, weakened across age. Model‐based comparisons revealed that for specific connections pubertal development described developmental change better than chronological age. This was particularly the case for changes in subcortical–cortical connectivity and distinctively for boys and girls. Together, these findings indicate changes in functional network strengthening with pubertal development. These changes in functional connectivity may maximize the neural efficiency of interregional communication and set the stage for further inquiry of biological factors driving adolescent functional connectivity changes.

AI snapshot

Written from the paper’s full text.

TL;DR

This three-wave longitudinal resting-state fMRI study found that subcortical–subcortical and cortico–cortical connectivity strengthened with age, whereas several subcortical–cortical connections weakened across adolescence into young adulthood. For specific connections, pubertal development described developmental change better than chronological age, with partly distinct patterns in boys and girls.

Key findings

  • In 661 scans from 273 participants aged 8–29 years, age-related strengthening occurred for subcortico-subcortical connections (e.g., amygdala–putamen, hippocampus–putamen, hippocampus–nucleus accumbens) and cortico-cortical connections (e.g., frontal medial–ventral ACC, frontal medial–dorsal ACC, subcallosal–ventral ACC).
  • Age-related decreases were observed only for subcortical–cortical connections, including caudate–dorsal ACC, hippocampus–dorsal ACC, nucleus accumbens–frontal medial cortex, nucleus accumbens–subcallosal cortex, and putamen–frontal medial cortex.
  • For boys, nucleus accumbens–frontal medial and putamen–frontal medial connectivity related negatively to Pubertal Development Scale (PDS) scores, while hippocampus–amygdala and subcallosal–dorsal ACC related positively; nucleus accumbens–frontal medial and subcallosal–dorsal ACC fit a PDS-only model better than an age-only model, and only hippocampus–amygdala remained significant over baseline age (p = .002).
  • For girls, hippocampus–dorsal ACC, caudate–dorsal ACC, and putamen–frontal medial connectivity related negatively to PDS; all three fit PDS-only better than age-only, and hippocampus–dorsal ACC (p = .006) and caudate–dorsal ACC (p = .02) remained significant over baseline age. Sex effects showed stronger hippocampus–amygdala connectivity in males and stronger hippocampus–ventral ACC connectivity in females; ICCs ranged from .08 to .33.

Methods

  • BrainTime three-wave accelerated longitudinal study; final sample was 661 observations from 273 participants (T1 n = 236, T2 n = 211, T3 n = 214), ages 8–29 years, with waves approximately 2 years apart. Resting-state fMRI was acquired on a 3.0 T Philips Achieva scanner; regions of interest came from the Harvard–Oxford atlas, including subcortical structures (nucleus accumbens, caudate, putamen, hippocampus, amygdala) and medial cortical regions (subcallosal cortex, frontal medial cortex, dorsal and ventral anterior cingulate cortex).
  • Preprocessing used FSL FEAT, motion correction and exclusion, FIX denoising, and white matter, CSF, and global signal regression; Pearson correlations were Fisher z-transformed. Generalized additive mixed models in R mgcv included random intercepts per participant; age, sex, and age × sex models were compared by BIC, and puberty models used PDS (participants under 18) separately by sex, compared with age-only models and with baseline age as a covariate; p-values were Bonferroni–Holm corrected.

Limitations

  • The paper states that resting-state connectivity is susceptible to motion; the authors excluded high-motion scans and used realignment parameters, tissue-specific signals, global signal regression, and FIX denoising, but note that FIX has mainly been applied in adults and that global signal regression can induce negative correlations and spurious results.
  • The paper states that using anatomical Harvard–Oxford ROIs rather than a functional brain atlas may be less sensitive for detecting age- or puberty-related change.
  • Evident from the text: PDS was only administered to participants under 18 and had missing data (405 data points; T1 n = 185, T2 n = 119, T3 n = 101), age and PDS were highly correlated, ICCs were low (.08–.33), and no explicit sex × puberty interaction was tested.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1002/hbm.24630

Cites

82 of 82 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

0 of 52 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    For specific connections, pubertal development described developmental change in resting-state connectivity better than chronological age.

    “Model‐based comparisons revealed that for specific connections pubertal development described developmental change better than chronological age.”
    Quote in the paperSubstantial claim
  • Findingown data

    Pubertal development and age were highly correlated at each time point (T1 r=.785, T2 r=.739, T3 r=.638).

    “Pubertal development and age were highly correlated at each time point: T1: r (185) = .785, p < .001; T2: r (129) = .739, p < .001; T3: r (101) = .638, p < .001.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Negative connectivity was observed between dorsal and ventral cortical regions, such as the dorsal ACC-subcallosal cortex and dorsal ACC-frontal medial cortex.

    “Negative connectivity was observed between dorsal and ventral cortical regions, such as the dorsal ACC–subcallosal cortex, and dorsal ACC–frontal medial cortex.”
    Quote in the paperNot a substantial claim
  • Findingown data

    In boys, the nucleus accumbens-frontal medial cortex and subcallosal cortex-dorsal ACC connectivity showed a better fit for a PDS-only than an age-only model when comparing BICs.

    “The nucleus accumbens‐frontal medial cortex and subcallosal cortex–dorsal ACC connectivity showed a better fit for a PDS‐only than an age‐only model when comparing BICs.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: PDS scores validly index pubertal development.
    • Rests on an assumption: PDS changes are most pronounced between ages 8 and 18.
  • Findingown data

    In boys, connectivity between the hippocampus-amygdala and subcallosal cortex-dorsal ACC was significantly positively related to PDS score, with increasing PDS being associated with increased RS connectivity.

    “Additionally, connectivity between the hippocampus‐amygdala (similar to age effects) and subcallosal cortex–dorsal ACC (not observed for age) was significantly positively related to PDS score, with increasing PDS being associated with increased RS connectivity.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: PDS scores validly index pubertal development.
    • Rests on an assumption: PDS changes are most pronounced between ages 8 and 18.
  • May combine two claims. 33
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 19

  • May combine two claims.

    Findingown data

    Visualization of significant age splines showed a relatively linear developmental pattern for all connections, with a few subcortical-cortical connections leveling off in adolescence or young adulthood.

    “Visualization of significant age splines showed a relatively linear developmental pattern for all connections, with a few subcortical–cortical connections leveling off in adolescence or young adulthood (see Figure 4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Functional connectivity between hippocampus-amygdala increased with age and was greater for males than females.

    “functional connectivity between hippocampus–amygdala increased with age and was greater for males than females (see Figure 4 plotted in red/blue, and Table 3).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Cortico-cortical connections showed a significant strengthening of connectivity with age between the frontal medial cortex-ventral ACC, frontal medial cortex-dorsal ACC, and between the subcallosal cortex-ventral ACC.

    “Cortico‐cortical connections also showed a significant strengthening of connectivity with age between the frontal medial cortex–ventral ACC, frontal medial cortex–dorsal ACC, and between the subcallosal cortex–ventral ACC (Figure 4b).”
    Quote in the paperSubstantial claim

  • The quote only partly states this claim.

    Findingown data

    Subcortical-cortical resting-state connectivity (e.g., nucleus accumbens-frontal medial cortex, caudate-dorsal anterior cingulate cortex) weakened with age.

    “Subcortical–cortical connectivity, such as, between the nucleus accumbens—frontal medial cortex, and the caudate—dorsal anterior cingulate cortex, however, weakened across age.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In a three-wave longitudinal sample aged 8-29, subcortico-subcortical and cortico-cortical resting-state functional connectivity strengthened with age.

    “We observed an age‐related strengthening of subcortico‐subcortical and cortico‐cortical connectivity.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The superiority of pubertal development over chronological age was particularly evident for subcortical-cortical connectivity and differed between boys and girls.

    “This was particularly the case for changes in subcortical–cortical connectivity and distinctively for boys and girls.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In boys, subcortical-cortical connectivity between the nucleus accumbens-frontal medial cortex and putamen-frontal medial cortex related negatively to PDS scores, with increasing PDS significantly decreasing RS connectivity.

    “For boys, subcortical–cortical connectivity between the nucleus accumbens–frontal medial cortex and putamen–frontal medial cortex related negatively to PDS scores, with increasing PDS significantly decreasing RS connectivity (similarly to what was observed for age) (see Figure 5; Table 4).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: PDS scores validly index pubertal development.
    • Rests on an assumption: PDS changes are most pronounced between ages 8 and 18.

  • May combine two claims.

    Findingown data

    Pubertal Development Scale scores were described by a main effect of sex and a spline effect of age, such that pubertal development manifested differently for boys and girls and increased with age.

    “Results showed that PDS score was described by a main effect of sex and spline effect of age. That is, pubertal development manifested differently for boys and girls and increased with age”
    Quote in the paperNot a substantial claim
    • The authors state this as an assumption: All participants completed pubertal development by 18 years.

  • May combine two claims.

    Findingown data

    Most regions were positively functionally connected, with the strongest positive connections between the amygdala-hippocampus and subcallosal cortex-frontal medial cortex.

    “Most regions were positively functionally connected, with the strongest positive connections between the amygdala–hippocampus and subcallosal cortex–frontal medial cortex.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    After correction for multiple comparisons, significant positive effects of age were observed for subcortical-subcortical connectivity between the amygdala, putamen, and hippocampus; between the putamen, nucleus accumbens, and hippocampus; and between the hippocampus and nucleus accumbens, all showing strengthening of functional connectivity with age.

    “After correction for multiple comparisons (Bonferroni–Holm), significant positive effects of age were observed for subcortical–subcortical connectivity between the amygdala, putamen, and hippocampus, between the putamen, nucleus accumbens, and hippocampus, and between the hippocampus and nucleus accumbens (Figure 4a), all showing a strengthening of functional connectivity with age.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Functional connectivity between the hippocampus-ventral ACC was not dependent on age, but was greater for females than males.

    “Functional connectivity between the hippocampus–ventral ACC was not dependent on age, but was greater for females than males.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The decrease in subcortical-cortical connectivity was unique, given that functional connectivity between subcortical and between cortical regions only strengthened with age.

    “The decrease in subcortical–cortical connectivity was unique, given that functional connectivity between subcortical and between cortical regions only strengthened with age.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    ICCs for RS connections ranged from 0.08 to 0.33, with most being at least above .1.

    “ICCs are listed in Table 2 and range from very poor (<.1) to poor (<.41) (Cicchetti, 1994).”
    • Also stated in: § Age‐related changes in functional connectivity · plain
      “the within‐individual stability was relatively low, with ICCs ranging between 0.08 and 0.33, although most being at least above .1 (e.g., Ordaz, Foran, Velanova, & Luna, 2013).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Connectivity patterns were highly stable across time points at the group level, with excellent within-sample replication of positive and negative connectivity patterns across three time points.

    “Our results showed, first, that connectivity patterns were highly stable across time points at the group level, with excellent within‐sample replication of positive and negative connectivity patterns across three time points.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Smooth splines can capture important nonlinear changes that are easily missed with polynomials, prevent biased fits at the extreme ranges of the data, while controlling Type 1 error rate.

    “Smooth splines can capture important nonlinear changes that are easily missed with polynomials, prevent biased fits at the extreme ranges of the data, while controlling Type 1 error rate in AIC/ Bayesian Information Criterion (BIC) values (Wood, 2017) and p‐values (Wood, 2013).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Wood, 2017

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    • cites Wood, 2013

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  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Few studies have yet examined connectivity in regions of the adolescent reward circuitry in a comprehensive maturational perspective.

    “However, few studies have yet examined connectivity in regions of the adolescent reward circuitry in a comprehensive maturational perspective.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisenone given

    Polynomial growth models assume age-related changes follow a restricted set of growth models.

    “a limitation of these models is that they assume age‐related changes follow this restricted set of growth models.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In resting-state studies, head motion may overestimate short-distance correlations and underestimate long-distance correlations.

    “as head motion may overestimate short‐distance correlations and underestimate long‐distance correlations (Power, Barnes, Snyder, Schlaggar, & Petersen, 2012; van Dijk, Sabuncu, & Buckner, 2012).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Power et al., 2012

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    • cites van Dijk et al., 2012

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  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    To date, no study has examined the relative contributions of age and puberty on functional connectivity changes.

    “However, to date, no study has examined the relative contributions of age and puberty on functional connectivity changes.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    All anatomical MRI scans were reviewed by a radiologist and no anomalous findings at any time point were reported.

    “All anatomical MRI scans were reviewed by a radiologist and no anomalous findings at any of the time points were reported.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Higher pubertal hormone concentrations were linked to a decrease in subcortical-prefrontal connectivity strength across typical adolescent development.

    “These studies highlighted that higher pubertal hormone concentrations were linked to a decrease in subcortical–prefrontal connectivity strength as seen across typical adolescent development.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Fareri et al., 2015

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    • cites Peters et al., 2015

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  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Reorganization of subcortical-cortical circuitry in adolescence is integral to adolescent development.

    “In sum, a reorganization of subcortical–cortical circuitry in adolescence is integral to adolescent development.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Previous studies of subcortical-cortical functional connectivity used different age samples, cross-sectional designs, and focused on single connections.

    “However, these studies used different age samples, cross‐sectional designs, and focused on single connections.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Fareri et al., 2015

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    • cites Padmanabhan et al., 2013

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    • cites Porter et al., 2015

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    Study design and conductown data

    FIX denoising resulted in a clear lowering of mean framewise displacement, and all included participants adhered to a more stringent FD cutoff of 0.2 mm on ≥2 volumes.

    “This resulted in a clear lowering of the mean FD (see Table 1). Note that for these cleaned time series, all included participants adhered even to a more stringent FD cutoff of 0.2 mm on ≥2 volumes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The amygdala and hippocampus are central regions for affective processing, aversive stimuli, and memory in adolescents, and are often coactivated with the medial PFC.

    “In addition, the amygdala and hippocampus are also central regions for respectively affective processing (e.g., Scherf, Smyth, & Delgado, 2013), processing aversive stimuli (Ernst, 2014), and memory (e.g., Davidow, Foerde, Galván, & Shohamy, 2016) in adolescents, and are often coactivated with the medial PFC.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Scherf et al., 2013

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    • cites Ernst, 2014

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    • cites Davidow et al., 2016

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

    Interpretationnone given

    The observed changes in functional connectivity may maximize the neural efficiency of interregional communication.

    “These changes in functional connectivity may maximize the neural efficiency of interregional communication”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The regions specified are part of subcortical and medial cortical reward regions typically implicated in functional reward processing and motivated behavior.

    “To examine functional connectivity patterns in adolescence, we specified regions as part of subcortical and medial cortical reward regions typically implicated in functional reward processing and motivated behavior (Doremus‐Fitzwater & Spear, 2016; Haber & Knutson, 2010; Telzer, 2016; van Duijvenvoorde, Achterberg, et al., 2016).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Doremus‐Fitzwater & Spear, 2016

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    • cites Haber & Knutson, 2010

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    • cites Telzer, 2016

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Regressing out global signal may reduce noise from physiological measures such as heart rate and respiration and differences in vigilance and arousal, yet it has been found to induce negative correlations and spurious results.

    “Regressing out global signal may reduce noise from physiological measures such as heart rate and respiration (Chen et al., 2012; Power et al., 2015) and differences in vigilance and arousal (Liu et al., 2017), yet it has been found to induce negative correlations and spurious results (Satterthwaite et al., 2013).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Chen et al., 2012

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    • cites Power et al., 2015

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    • cites Liu et al., 2017

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Previous studies have suggested that pubertal development may advance or enhance growth trajectories of brain development.

    “Previous studies focusing on functional reactivity have often suggested that pubertal development may advance or enhance growth trajectories of brain development, although most studies up to now focused on brain structural development (e.g., Herting & Sowell, 2017; Vijayakumar, Mills, Alexander‐Bloch, Tamnes, & Whittle, 2018) or cross‐sectional functional connectivity development (Fareri et al., 2”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Herting & Sowell, 2017

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    • cites Vijayakumar, Mills, Alexander‐Bloch, Tamnes, & Whittle, 2018

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    • cites Fareri et al., 2015

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  • May combine two claims.

    Study design and conductcitation

    The current study took steps to account for motion confounds, including excluding participants above a set motion threshold and including realignment parameters, tissue-specific signals, global signal regression, and FSL FIX denoising.

    “In the current study, we have taken steps to account for such possible confounds (see Satterthwaite et al., 2017).”
    • Also stated in: § Limitations · plain
      “Specifically, we first excluded people above our set motion threshold. Further, we included realignment parameters, tissue‐specific signals, global signal regression, and a denoising procedure based on an independent components analyses (FSL FIX).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Satterthwaite et al., 2017

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  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    The p-values of fixed effects in all best-fitting models were corrected for multiple comparisons with a Bonferroni-Holm correction and evaluated at p < .05.

    “The p‐values of fixed effects in all best‐fitting models were corrected for multiple comparisons with a Bonferroni–Holm correction and evaluated at p < .05.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In humans, decreases in gray matter density in frontal regions, as well as hippocampus, amygdala, and caudate volumes, have been related to pubertal development.

    “In humans, decreases in gray matter density in frontal regions (Peper et al., 2009), as well as hippocampus, amygdala, and caudate volumes (Goddings et al., 2014; Wierenga et al., 2018) have been related to pubertal development”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Peper et al., 2009

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    • cites Goddings et al., 2014

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    • cites Wierenga et al., 2018

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  • May combine two claims.

    Interpretationown data

    The developing efficiency of the brain is a puberty-driven maturational process that may accelerate changes in modularity and plasticity in the developing brain.

    “suggesting that the developing efficiency of the brain is a puberty‐driven maturational processes that may accelerate changes in modularity and plasticity in the developing brain.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Previous research on sex differences has mostly been done in adults and has shown higher hippocampal and/or amygdala connectivity in females than males.

    “Previous research on sex differences has mostly been done in adults (e.g., Alarcón, Cservenka, Rudolph, Fair, & Nagel, 2015; Kogler et al., 2016), and has shown higher hippocampal and/or amygdala connectivity in females than males”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Alarcón et al., 2015

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    • cites Kogler et al., 2016

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    • cites Gur & Gur, 2016

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  • May combine two claims.

    Interpretationown data

    Pubertal development in boys and girls has differential influence on subcortical-cortical connectivity, decreasing connectivity in both sexes but affecting different connections.

    “These differences between sexes may suggest that pubertal development in boys and girls has differential influence on the development of subcortical–cortical connectivity.”
    • Also stated in: § Age‐ versus puberty‐related changes in functional connectivity · hedged
      “Although we did not explicitly test for sex × pubertal developmental interactions, our findings seem to indicate that pubertal development decreases connectivity in both girls and boys, yet affects different subcortical–cortical connections.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Animal work has observed a reduction in medial PFC volume and synapses in postpubertal rats, and neuronal losses during pubertal onset.

    “animal work has observed a reduction in medial PFC volume and synapses in postpubertal rats, and neuronal losses during pubertal onset (Walker et al., 2017; Willing & Juraska, 2015).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Walker et al., 2017

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    • cites Willing & Juraska, 2015

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  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    The use of these denoising techniques may be especially helpful in cleaning relatively noisy data from such specific populations, and can improve signal and analysis quality.

    “However, the use of these denoising techniques may be especially helpful in cleaning relatively noisy data from such specific populations, and can improve signal and analysis quality.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Previous work showed that structural networks become more segregated across development, and that BOLD dimensionality decreases with age.

    “Previous work also showed that structural networks become more segregated across development (Baum, Ciric, Roalf, Betzel, et al., 2017), and that BOLD dimensionality decreases with age (Kundu et al., 2018).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Baum, Ciric, Roalf, Betzel, et al., 2017

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    • cites Kundu et al., 2018

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  • May combine two claims.

    Interpretationown data

    The findings may be interpreted as change in local versus distributed networks in which specific functional networks both strengthen and weaken across adolescence.

    “Together, these findings may be interpreted as change in local versus distributed networks in which specific functional networks both strengthen and weaken across adolescence.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    The study used an anatomical atlas (Harvard-Oxford) that may allow for more specific cortical regions.

    “Here, we used an anatomical atlas that may allow for more specific cortical regions by choosing a standardized structural probabilistic atlas, namely the Harvard–Oxford atlas.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    This lower homogeneity is particularly so for atlases that use large structural regions such as the AAL, while more fine-grained structural atlases such as Brodmann areas seem to perform better.

    “This is particularly so for atlases that use large structural regions such as the AAL (Gordon et al., 2014), while more fine‐grained structural atlases such as Brodmann areas seem to perform better.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gordon et al., 2014

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    Premisecitation

    Using anatomical ROIs versus a functional brain atlas may be less sensitive in detecting age- or puberty-related change.

    “Using anatomical ROIs versus a functional brain atlas (such as the areal atlas of Power et al., 2011) may be less sensitive in detecting age‐ (or puberty) related change.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Power et al., 2011

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The advantage of structural atlases is that they are highly standardized and used typically in both developmental functional imaging studies and RS studies.

    “The advantage of structural atlases is that they are highly standardized, and used typically in both developmental functional imaging studies (e.g., Achterberg et al., 2018) and RS studies (e.g., Fareri et al., 2015; Stevens, 2016).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Achterberg et al., 2018

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    • cites Fareri et al., 2015

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    • cites Stevens, 2016

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    Study design and conductcitation

    The study included global signal regression to benefit from reduction in artifacts and to build on prior developmental studies.

    “Thus, to benefit from the reduction in artifacts, as well as to build on prior developmental studies (Fareri et al., 2015; Gabard‐Durnam et al., 2014; Peters et al., 2015; Peters, Peper, et al., 2016; Peters, van Duijvenvoorde, Koolschijn, & Crone, 2016; van Duijvenvoorde, Achterberg, et al., 2016), we opted to also include a global signal regression.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Fareri et al., 2015

      Not checked in the free run.

    • cites Gabard-Durnam et al., 2014

      Not checked in the free run.

    • cites Peters et al., 2015

      Not checked in the free run.

44 of 44

  • The authors state this as an assumption.

    All participants completed pubertal development by 18 years.

    “because it was assumed that all participants completed pubertal development by 18 years.”

  • The paper relies on this without support.

    The Harvard–Oxford atlas is an often used and well-known atlas in functional brain analyses.

    “Although based on anatomical parcellation, the Harvard–Oxford atlas is an often used and well‐known atlas in functional brain analyses.”

  • The paper relies on this without support.

    The ventral striatum, and particularly the nucleus accumbens, is a key structure for reward processing.

    “The ventral striatum, and particularly the nucleus accumbens, is considered a key structure for reward processing.”

  • The paper relies on this without support.

    The medial prefrontal cortex is densely connected to the ventral striatum and is a crucial regulator of reward-directed behavior.

    “The medial prefrontal cortex (PFC) is densely connected to the ventral striatum and suggested to be a crucial regulator of reward‐directed behavior.”

  • The paper relies on this without support.

    The ventral striatum together with nuclei in the amygdala, parts of the hippocampus, and the medial PFC form a larger circuitry that modulates responses to salient stimuli and drives reward learning and decision-making.

    “Thus, the ventral striatum together with nuclei in the amygdala, parts of the hippocampus, and the medial PFC, form a larger circuitry that modulate responses to salient stimuli and drive reward learning and decision‐making.”

  • The paper relies on this without support.

    PDS scores validly index pubertal development.

    “To assess effects of puberty on RS connectivity, models were assessed separately for boys and girls, given that puberty had different timings in males and females (see Wierenga et al., 2018 for an example on structural brain development and pubertal development).”
    “we observed that a number of subcortical–cortical connections sensitive to developmental change were better described by (self‐reported) pubertal development than age.”

  • The paper relies on this without support.

    Age and PDS are highly collinear.

    “Due to the high collinearity between age and PDS, we opted for age at baseline (Equation (7)).”

  • The paper relies on this without support.

    PDS changes are most pronounced between ages 8 and 18.

    “only including participants between ages 8 and 18‐years old, during which PDS changes are most pronounced.”
8 of 8

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • Consistentr(185) = 0.785reported p < .001 · recomputed p < .001

    “r (185) = .785, p < .001”

  • Consistentr(129) = 0.739reported p < .001 · recomputed p < .001

    “r (129) = .739, p < .001”

  • Consistentr(101) = 0.638reported p < .001 · recomputed p < .001

    “r (101) = .638, p < .001”

  • Consistentr(236) = -0.142reported p = .029 · recomputed p = .029

    “r (236) = −.142, p = .029”

  • Consistentr(213) = -0.15reported p = .025 · recomputed p = .028

    “r (213) = −.15, p = .025”

5 of 5

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Self-check results appear here once an independent check has confirmed them.

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. R Core Team, 2017, R: A language and environment for statistical computing. R Foundation for Statistical Computing
  2. Wechsler D., 1974, Wechsler intelligence scale for children – Revised (WISC R)

Cited by

Sorted by citations

Related

Authors
van Duijvenvoorde, A. C. K., Westhoff, B., de Vos, F., Wierenga, L. M., & Crone, E. A.
Affiliations
  • Institute of Psychology Leiden University Leiden The Netherlands
  • Leiden University (NL)
ORCID
Venue
Human Brain Mapping
Publisher
Wiley
Published
2019-05-17
Volume
40
Issue
13
Pages
3769-3783
ISSN
  • 1065-9471 (ISSN-L)
  • 1097-0193
DOI
10.1002/hbm.24630
PMC
PMC6767490
OpenAlex
W2946376327
Cited by
115
References
82
Citations by year
2026: 16 · 2025: 15 · 2024: 14 · 2023: 18 · 2022: 17 · 2021: 19 · 2020: 14 · 2019: 2
FWCI
7.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Human Brain Mapping (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Leiden Repository (Leiden University) (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
  • Leiden Repository (Leiden University) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
European Research Council Starting Grant (ERC-2010-StG_263234)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
resting-state functional connectivity, adolescence, puberty, medial prefrontal cortex, nucleus accumbens, caudate nucleus, putamen, hippocampus, amygdala, anterior cingulate cortex, subcallosal cortex, sex differences, age-related changes, neural efficiency
MeSH terms
Adolescent, Adult, Child, Female, Humans, Human Development, Longitudinal Studies, Magnetic Resonance Imaging, Male, Nerve Net, Puberty, Adolescent Development, Cerebrum, Young Adult, Connectome

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 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

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