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Longitudinal Working Memory Development Is Related to Structural Maturation of Frontal and Parietal Cortices

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Longitudinal Working Memory Development Is Related to Structural Maturation of Frontal and Parietal Cortices Longitudinal Working Memory Development Is Related to Structural Maturation of Frontal and Parietal Cortices Christian K. Tamnes1, Kristine B. Walhovd1, Håkon Grydeland1, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/25/10/1611/1779760/jocn_a_00434.pdf by MIT Libraries user on 17 May 2021 Dominic Holland2, Ylva Østby1, Anders M. Dale2, and Anders M. Fjell1 Abstract ■ Parallels between patterns of brain maturation and cognitive points in 79 healthy children and adolescents in the age range development have been observed repeatedly, but studies directly of 8–22 years. Longitudinal change in cortical and subcortical testing the relationships between improvements in specific cog- volumes was quantified by the use of Quantitative Anatomical nitive functions and structural changes in the brain are lacking. Regional Change. Improvement in working memory was related Working memory development extends throughout childhood to cortical volume reduction in bilateral prefrontal and posterior and adolescence and likely plays a central role for cognitive devel- parietal regions and in regions around the central sulci. Impor- opment in multiple domains and in several neurodevelopmental tantly, these relationships were not explained by differences in disorders. Neuroimaging, lesion, and electrophysiological studies gender, age, or intelligence level or change in intellectual abil- indicate that working memory emerges from coordinated inter- ities. Furthermore, the relationships did not interact with age actions of a distributed neural network in which fronto-parietal and were not significantly different in children, young adoles- cortical regions are critical. In the current study, verbal working cents, and old adolescents. The results provide the first direct memory function, as indexed by performance on the Keep Track evidence that structural maturation of a fronto-parietal cortical task, and volumes of brain regions were assessed at two time network supports working memory development. ■ INTRODUCTION ning in lateral dorsal frontal and parietal regions in the left Cognitive development in childhood and adolescence is hemisphere (LH). However, no previous studies have the result of a dynamic interaction between maturation attempted to map change in specific cognitive functions and learning, and parallels between patterns of brain directly to the maturation of specific brain networks. Here, maturation and cognitive development have been ob- we test the relationships between change in verbal working served (Lebel & Beaulieu, 2011; Gogtay et al., 2004). Still, memory performance and change in cortical and sub- aside from two notable exceptions focusing on general cortical volumes in a group of children and adolescents. cognitive abilities (Shaw et al., 2006; Sowell et al., 2004), Working memory, conceptualized as a limited capacity there is a lack of longitudinal studies directly linking cog- multicomponent system for the temporary maintenance nitive functions and brain structure in development. In and manipulation of information (Baddeley, 2012), is an a large sample of children and adolescents, Shaw et al. interesting candidate for testing the relationships between (2006) found that the trajectory of change in the cerebral development of specific cognitive functions and structural cortex, rather than the cortical morphology itself, was most brain maturation for several reasons. First, working mem- closely related to the level of intelligence. The results in- ory performance is known to improve throughout child- dicated that children at different levels of intelligence had hood and adolescence (Conklin, Luciana, Hooper, & different cortical maturational trajectories, primarily in Yarger, 2007; Waber et al., 2007; Gathercole, Pickering, frontal regions, and that children with higher intelligence Ambridge, & Wearing, 2004; Luna, Garver, Urban, Lazar, scores had a more plastic cortex. Sowell et al. (2004) tested & Sweeney, 2004) and to be predictive of scholastic attain- the relationships between change in both behavioral per- ment (Alloway & Alloway, 2010; Hitch, Towse, & Hutton, formance and cortical structure in a group of children fol- 2001). Second, working memory supports other cognitive lowed over 2 years and found that those who improved processes by providing an interface between perception, more in verbal intellectual ability had greater cortical thin- long-term memory, and action (Baddeley, 2012) and is therefore of central importance for cognitive develop- ment in multiple domains. Third, deficits in working 1University of Oslo, Norway, 2University of California, San Diego memory are observed in many neurodevelopmental © 2013 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 25:10, pp. 1611–1623 doi:10.1162/jocn_a_00434 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00434 by guest on 29 September 2021 disorders, including attention-deficit hyperactivity dis- providing bidirectional information transfer between the order and schizophrenia (Forbes, Carrick, McIntosh, & frontal and parietal cortices (Yeterian, Pandya, Tomaiuolo, Lawrie, 2009; Martinussen, Hayden, Hogg-Johnson, & & Petrides, 2012), and the latter results thus elaborate the Tannock, 2005). Finally, a large number of neuroimaging, evidence for the involvement of a fronto-parietal network lesion, and electrophysiological studies provide a tentative in working memory. These age-independent associations mapping of working memory onto a network of anatomical are presumably partly mediated by variability in the pace localizations (Sander, Lindenberger, & Werkle-Bergner, of brain maturation ( Jernigan, Baare, Stiles, & Madsen, 2012; DʼEsposito, 2007; Linden, 2007; Muller & Knight, 2011), but longitudinal studies are needed to directly test Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/25/10/1611/1779760/jocn_a_00434.pdf by MIT Libraries user on 17 May 2021 2006; Baddeley, 2003). the relationships between working memory development Functional imaging studies using a variety of tasks have and brain maturation. implicated a distributed network of brain regions, including This study addresses the following specific questions: prefrontal and posterior parietal cortices as well as pri- (1) Is working memory development related to changes mary cortical areas, in working memory functions in both in cortical and subcortical volumes during childhood and adults (Burzynska et al., 2011; Nagel et al., 2011; Collette adolescence? (2) Do these relationships interact with et al., 2005; Owen, McMillan, Laird, & Bullmore, 2005; age? As no prior longitudinal studies have explored how Gerton et al., 2004; Wager & Smith, 2003; Cabeza & working memory development relates to brain structure Nyberg, 2000) and children and adolescents (OʼHare, Lu, changes, we performed analyses both across the cortical Houston, Bookheimer, & Sowell, 2008; Crone, Wendelken, surface and in a large number of subcortical structures. Donohue, van Leijenhorst, & Bunge, 2006; Klingberg, 2006; On the basis of the above-described functional imaging Scherf, Sweeney, & Luna, 2006; Olesen, Nagy, Westerberg, studies and studies showing gray-matter volume decreases & Klingberg, 2003; Klingberg, Forssberg, & Westerberg, in most regions in adolescence (Tamnes et al., 2013; Østby 2002; Kwon, Reiss, & Menon, 2002). Overall, a general et al., 2009; Lenroot et al., 2007), we hypothesized that similarity of the cortical regions at work in children and improvement in working memory performance would be adults is indicated (Thomason et al., 2009). Some studies associated with volume reduction in the network of pre- have also found working memory recruitment of sub- frontal and posterior parietal cortices supporting working cortical structures, including BG (Moore, Li, Tyner, Hu, & memory function as well as in BG structures. Furthermore, Crosson, 2013; Podell et al., 2012; Chang, Crottaz-Herbette, because cognitive development and brain maturation & Menon, 2007; Olesen, Nagy, Westerberg, & Klingberg, generally are more rapid at younger age, we tentatively 2003), hippocampus (Finn, Sheridan, Kam, Hinshaw, & also hypothesized that the relationships would vary with DʼEsposito, 2010), and cerebellum (Ciesielski, Lesnik, Savoy, age and be stronger in children than in adolescents. Grant, & Ahlfors, 2006), possibly with diminishing contribu- tions with age in development. Throughout childhood and adolescence, the brain METHODS undergoes a multifaceted and regionally differentiated maturational process. Magnetic resonance imaging (MRI) Participants studies have documented considerable developmental The sample was drawn from the longitudinal research proj- structural changes in cerebral cortex and subcortical and ect “Neurocognitive Development” (Tamnes et al., 2013), cerebellar structures (Tamnes et al., 2013; Brown et al., University of Oslo. The study was approved by the Re- 2012; van Soelen et al., 2012; Sullivan et al., 2011; Tiemeier gional Committee for Medical and Health Research Ethics. et al., 2010; Shaw et al., 2008; Lenroot et al., 2007) as well Children and adolescents aged 8–19 years were recruited as volumetric increases and microstructural changes, as through newspaper ads and local schools. Written in- indexed by diffusion tensor imaging, in white matter (Lebel formed consent was obtained from all participants older & Beaulieu, 2011; Tamnes, Østby, Fjell, et al., 2010; Westlye than 12 years old and from a parent of participants under et al., 2010).
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