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  • Developmental Cognitive Neuroscience 10 (2014) 148159

    Contents lists available at ScienceDirect

    Developmental Cognitive Neuroscience

    journa l homepage: ht tp : / /www.e lsev ier .com/ locate /dcn

    Development of the Default Mode and Central ExecutiveNetworks across early adolescence: A longitudinal study

    Lauren E. Shermana,b,, Jeffrey D. Rudieb, Jennifer H. Pfeiferc, Carrie L. Mastenb,Kristin McNealyb, Mirella Daprettob,d

    a Department of Psychology, University of California, Los Angeles, Los Angeles, CA, USAb Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles, Los Angeles, CA, USAc Department of Psychology, University of Oregon, Eugene, OR, USAd Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, USA

    a r t i c l e i n f o

    Article history:Received 6 June 2014Received in revised form 31 July 2014Accepted 6 August 2014Available online 20 August 2014

    Keywords:Adolescent brain developmentFunctional connectivityDefault Mode NetworkCentral Executive NetworkIntelligenceEarly adolescence

    a b s t r a c t

    The mature brain is organized into distinct neural networks defined by regions demonstrat-ing correlated activity during task performance as well as rest. While research has begunto examine differences in these networks between children and adults, little is knownabout developmental changes during early adolescence. Using functional magnetic reso-nance imaging (fMRI), we examined the Default Mode Network (DMN) and the CentralExecutive Network (CEN) at ages 10 and 13 in a longitudinal sample of 45 participants.In the DMN, participants showed increasing integration (i.e., stronger within-networkcorrelations) between the posterior cingulate cortex (PCC) and the medial prefrontal cor-tex. During this time frame participants also showed increased segregation (i.e., weakerbetween-network correlations) between the PCC and the CEN. Similarly, from age 10 to13, participants showed increased connectivity between the dorsolateral prefrontal cortexand other CEN nodes, as well as increasing DMN segregation. IQ was significantly positively

    related to CEN integration at age 10, and between-network segregation at both ages. Thesefindings highlight early adolescence as a period of significant maturation for the brainsfunctional architecture and demonstrate the utility of longitudinal designs to investigateneural network development. 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC

    Y-NC-N

    B

    1. Introduction

    Early adolescence is a period of substantial neural devel-opment, triggered in part by biological changes relatedto the onset of puberty as well as significant changes in

    youths social sphere. Work in animals and neuroimagingstudies in humans suggest that pubertal development cor-responds with significant changes in the brains structural

    Corresponding author at: 1285 Franz Hall, Box 951563, Los Angeles,CA 90095-1563, United States. Tel.: +1 215 317 4447.

    E-mail address: lsherman@ucla.edu (L.E. Sherman).

    http://dx.doi.org/10.1016/j.dcn.2014.08.0021878-9293/ 2014 The Authors. Published by Elsevier Ltd. This is an open accelicenses/by-nc-nd/3.0/).

    D license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

    and functional organization (e.g., Blakemore et al., 2010;Sato et al., 2008). This neural maturation is accompaniedby developments in the social and cognitive domains. Ado-lescents experience a social reorientation (Nelson et al.,2005) whereby they become increasingly sensitive to socialcues and peer relationships. Indeed, the emphasis on sociallearning and preparation for adult roles during adolescenceoccurs in cultures around the world (Schlegel and Barry,1991; Schlegel, 1995). Youth also make important strides

    in executive functioning, including inhibitory control, plan-ning for the future, metacognition, and hypothesizingabout others mental states (e.g., Dumontheil et al., 2010;Weil et al., 2013; Williams et al., 1999).

    ss article under the CC BY-NC-ND license (http://creativecommons.org/

    dx.doi.org/10.1016/j.dcn.2014.08.002http://www.sciencedirect.com/science/journal/18789293http://www.elsevier.com/locate/dcnhttp://crossmark.crossref.org/dialog/?doi=10.1016/j.dcn.2014.08.002&domain=pdfhttp://creativecommons.org/licenses/by-nc-nd/3.0/mailto:lsherman@ucla.edudx.doi.org/10.1016/j.dcn.2014.08.002http://creativecommons.org/licenses/by-nc-nd/3.0/http://creativecommons.org/licenses/by-nc-nd/3.0/

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    L.E. Sherman et al. / Developmental

    Between childhood and adulthood, significant changeslso occur in the functional architecture of the brain.he adult human brain is organized into functionaletworks, consisting of sets of distinct neural regionshat demonstrate correlated blood oxygen level-dependentBOLD) signal fluctuations both during specific tasks andhile at rest (e.g., Fox and Raichle, 2007). Immature

    ersions of these networksi.e., significant but weakeronnectivity between some or all hub regions of eachetworkhave been documented in childhood and even,o some extent, in infancy (for a review, see Dennis andhompson, 2013). Nonetheless, these immature networksend to have weaker internal connectivity and areess functionally segregated (i.e., demonstrate strongeretween-network correlation) than those in adulthood,ith adolescence representing a period of intermediate

    onnectivity (Jolles et al., 2011; Kelly et al., 2009; Fair et al.,007a, 2009; Hwang et al., 2013). Despite our increas-

    ng understanding of the dramatic neural maturation thatccurs during the second decade of life, relatively less isnown about the development of functional networks dur-

    ng adolescence, particularly during the years when theost dramatic pubertal changes typically occur. Further-ore, the majority of research examining the maturation of

    unctional networks has relied upon cross-sectional, ratherhan longitudinal data, with only a few exceptions in infantopulations (e.g., Gao et al., 2014; Smyzer et al., 2010).he present study examines the development of two func-ional networks in early adolescence using a longitudinalample of participants who were studied at ages 10 and3. Specifically we examined the Default Mode NetworkDMN) and the Central Executive Network (CEN), whichave been implicated in social cognition and executive con-rol, respectively.

    Raichle and colleagues (2001) first observed that a net-ork of neural regions, including the posterior cingulate

    ortex (PCC), the medial prefrontal cortex (mPFC), andhe lateral parietal cortex showed increased activity dur-ng baseline, or when an individual is at rest. This sameetwork of regions has been shown to be deactivated dur-

    ng a variety of neuroimaging tasks requiring cognitiverocessing; indeed, it has also been labeled the task-egative network (Fox et al., 2005b; Greicius et al., 2003;inder et al., 1999; Shulman et al., 1997). The past decadeas seen a surge of scientific interest in the DMN, both inypical and clinical populations (for a review, see Broydt al., 2009). In task-based fMRI designs, regions of the DMNre frequently activated during social cognition, includingrocessing emotional stimuli, introspection, and thinkingbout others mental states (e.g., Blakemore, 2008; Gusnardt al., 2001; Maddock, 1999). Given its involvement in socialognition, this network of regions is sometimes referred tos the mentalizing network in the social affective neuro-cience literature (e.g., Atique et al., 2011).

    The CEN, in contrast, is one of the two networks thatrequently activates during typical fMRI tasks involvingxecutive functions. Seeley and colleagues (2007) dis-

    inguished between the salience network, with mainubs in the dorsal anterior cingulate and orbitofrontal

    nsular cortices, and the CEN, anchored in the dorsolateralrefrontal cortex (dlPFC) and posterior parietal cortex

    e Neuroscience 10 (2014) 148159 149

    (pPC), particularly the intraparietal sulcus (IPS). Theyreported that activity in the CEN, but not the saliencenetwork, correlated with performance on executivecontrol tasks. Emerging evidence suggests the strengthof within-network connectivity in the CEN, (also calledthe frontoparietal control system/network; Vincent et al.,2008) is associated with higher IQ in children, adolescents,and adults (e.g., Langeslag et al., 2013; Li and Tian, 2014;Song et al., 2008). CEN activity has been shown to beanticorrelated with activity in the DMN in healthy adults(Fox et al., 2005b; Menon and Uddin, 2010; Sridharan et al.,2008), and it has been proposed that it may even directlyinhibit DMN activity under certain circumstances (Chenet al., 2013). Data from cross-sectional research suggeststhat increasing integration within each functional networkand segregation between these and other networks occursthroughout childhood and adolescence (Fair et al., 2007a).

    The present study aimed to investigate the integrationand segregation of the CEN and DMN during a relativelynarrow period of developmentages 10 to 13whereinsignificant structural and functional brain maturation, aswell as socioemotional and cognitive development, occur.The data were collected as part of a longitudinal studywhich did not involve a traditional resting-state scan.Instead, we used functional data from a passive listeningtask of meaningless speech (McNealy et al., 2006, 2010,2011) and performed the analyses on a residual timeseriesafter the task-specific effects were statistically controlledfor. While our fMRI scan does differ somewhat from atraditional resting state scan, it is worth noting that par-ticipants were not engaging in active semantic processing,as the auditory stimulus was composed of

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