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Neurodevelopmental Correlates of the Emerging Adult Self T ⁎ Christopher G Developmental Cognitive Neuroscience 36 (2019) 100626 Contents lists available at ScienceDirect Developmental Cognitive Neuroscience journal homepage: www.elsevier.com/locate/dcn Neurodevelopmental correlates of the emerging adult self T ⁎ Christopher G. Daveya,b,c, , Alex Fornitod,e, Jesus Pujolf, Michael Breakspearg,h, Lianne Schmaala,b, Ben J. Harrisonc a Orygen, The National Centre of Excellence in Youth Mental Health, Parkville, Australia b Centre for Youth Mental Health, The University of Melbourne, Parkville, Australia c Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne, Parkville, Australia d Monash Clinical and Imaging Neuroscience, School of Psychological Sciences, Monash University, Clayton, Australia e Monash Biomedical Imaging, Monash University, Clayton, Australia f MRI Research Unit, Department of Radiology, Hospital del Mar, CIBERSAM G21, Barcelona, Spain g QIMR Berghofer Medical Research Institute, Brisbane, Australia h Hunter Medical Research Institute, University of Newcastle, Newcastle, Australia ARTICLE INFO ABSTRACT Keywords: The self-concept – the set of beliefs that a person has about themselves – shows significant development from Adolescent development adolescence to early adulthood, in parallel with brain development over the same period. We sought to in- Connectivity vestigate how age-related changes in self-appraisal processes corresponded with brain network segregation and Default mode network integration in healthy adolescents and young adults. We scanned 88 participants (46 female), aged from 15 to 25 Functional MRI years, as they performed a self-appraisal task. We first examined their patterns of activation to self-appraisal, and Self replicated prior reports of reduced dorsomedial prefrontal cortex activation with older age, with similar re- ductions in precuneus, right anterior insula/operculum, and a region extending from thalamus to striatum. We used independent component analysis to identify distinct anterior and posterior components of the default mode network (DMN), which were associated with the self-appraisal and rest-fixation parts of the task, respectively. Increasing age was associated with reduced functional connectivity between the two components. Finally, analyses of task-evoked interactions between pairs of nodes within the DMN identified a subnetwork that de- monstrated reduced connectivity with increasing age. Decreased network integration within the DMN appears to be an important higher-order maturational process supporting the emerging adult self. 1. Introduction comprises a set of regions that shows greater activity and functional coupling when a person is in a task-free ‘resting-state’, but also when One of the key developmental tasks during the transition to adult- engaged in task-oriented forms of self-referential processing (Andrews- hood is the establishment of a more coherent self-structure (Arnett and Hanna et al., 2014; Raichle et al., 2001; Harrison et al., 2008, 2011). Taber, 1994; Harter, 2006). The self-concept – or the set of beliefs that a The core DMN regions are the dorsal and ventral medial prefrontal person has about themselves – becomes more clearly defined during cortex, the posterior cingulate cortex, and the inferior parietal lobule, adolescence, supporting a young person’s emerging independence but other regions are also (inconsistently) included (Buckner et al., (Harter, 1990; Demo, 1992). The cortical regions that support self-re- 2008). Functional magnetic resonance imaging (fMRI) studies show presentations develop along a similar timeframe, reaching full maturity that anterior components of the DMN, especially the dorsal medial in the third decade of life (Gogtay et al., 2004; Lebel and Beaulieu, prefrontal cortex (DMPFC), have particular involvement in self-ap- 2011). Both the self-concept and corresponding brain regions develop praisal processes (including those that occur during resting-state in- together, but in a relationship that remains incompletely understood. trospection); while posterior DMN regions have greater involvement in Self-appraisal – one’sreflection on the attributes of the self-concept other resting-state processes, such as low-level surveillance of the ex- – activates mainly midline cortical regions in a pattern that overlaps ternal and internal environment (Davey et al., 2016; Whitfield-Gabrieli with the default mode network (DMN) (Davey et al., 2016). The DMN et al., 2011; D’Argembeau et al., 2005; Gusnard et al., 2001). Model- ⁎ Corresponding author at: Orygen, The National Centre of Excellence in Youth Mental Health & Centre for Youth Mental Health, The University of Melbourne, 35 Poplar Rd., Parkville, Victoria, 3052, Australia. E-mail address: [email protected] (C.G. Davey). https://doi.org/10.1016/j.dcn.2019.100626 Received 12 July 2018; Received in revised form 29 January 2019; Accepted 13 February 2019 Available online 16 February 2019 1878-9293/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). C.G. Davey, et al. Developmental Cognitive Neuroscience 36 (2019) 100626 free analyses of resting-state fMRI data often separates the DMN into which examined the differences and commonalities between brain re- anterior and posterior components (Allen et al., 2011; Kalcher et al., gions activated during self-appraisal and rest; and were also included as 2012; Damoiseaux et al., 2006; Kim and Lee, 2011) – supporting a the control group in our examination of self-appraisal in depression segregation of their interconnected functions. (Davey et al., 2017). While the relationship between development of the brain and psy- chological aspects of the self remains uncertain, one aspect has been 2.2. Paradigm design consistently demonstrated (Blakemore, 2012): during the transition from adolescence to early adulthood there is reduced activation in the Participants completed a single run of an fMRI task composed of DMPFC in response to presentation of self-related stimuli (Pfeifer et al., three alternating experimental conditions: self-appraisal, external at- 2007, 2009; Blakemore et al., 2007; Sebastian et al., 2012). It has been tention, and rest-fixation. In the self-appraisal condition, participants ffi speculated that brain maturation leads to greater e ciency of neural were presented with a personality adjective and asked whether or not processing, such that less DMPFC activity is required to perform self- the word described them. Words were drawn from a frequently used list appraisal tasks over the course of development (Sebastian et al., 2008). of personality adjectives (Anderson, 1968), and included words with An increased research focus on the interaction of large-scale brain relatively neutral valence ratings: words such as ‘skeptical’, ‘perfectio- systems has brought a network-based perspective to neurodevelop- nistic’, and ‘lucky’ (see Davey et al., 2016). Participants viewed eight mental processes (Baker et al., 2015; Power et al., 2010; Kaufmann blocks of six words, presented for 5 s each, and responded to the et al., 2017). Resting-state fMRI studies comparing children (7- to 9- question, ‘Does this word describe you?’, by pressing the left or right year-olds) to adults (21- to 31-year-olds in one study and 19- to 22-year- button on the fiber-optic response pad. In the external attention con- olds in another) have shown a pattern of increasing resting-state DMN dition, participants viewed eight blocks of six words, also presented for connectivity with development (Fair et al., 2008; Supekar et al., 2010). 5 s each, and responded to the question, ‘Does this word have four or In opposition to this, decreased resting-state connectivity between more vowels?’ (Supplementary Fig. 2). anterior and posterior DMN components has been observed to accom- The two lists of 48 words that formed the self-appraisal and external pany the transition from adolescence to early adulthood in a cohort of attention conditions were matched on valence ratings and number of 12- to 30-year-olds (Stevens et al., 2009). While there is, therefore, vowels, and their presentation was counterbalanced across participants. uncertainty as to whether DMN connectivity shows functional in- Each 32 s block (2 s instruction followed by six words presented for 5 s tegration or segregation during adolescent development, the con- each) was interspersed with a 10 s rest-fixation block in which parti- nectivity changes are likely to be relevant to the development of the cipants were asked to fixate on a centrally presented cross-hair. fi self-concept, and need clari cation. Behavioral data (accuracy and response-times) were analyzed with The objective of the present study was to investigate the neural Stata 15 (StataCorp, College Station, USA). correlates of the developing self-concept across adolescence and early adulthood. In particular, we sought to quantify developmental asso- ciations with functional network connectivity, with a particular focus 2.3. Image acquisition on the DMN. We first examined age-dependent changes in brain acti- vation during self-appraisal to test the replicability of previous findings A 3 T General Electric Signa Excite system equipped with an eight- of decreased DMN activation to self-referential stimuli. We then sought channel phased-array head coil was used in combination with ASSET to examine the development of DMN connectivity, both at the level of parallel imaging. The functional sequence consisted
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