Functional Brain Connectivity at Rest Changes After Working Memory Training

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Functional Brain Connectivity at Rest Changes After Working Memory Training r Human Brain Mapping 00:000–000 (2011) r Functional Brain Connectivity at Rest Changes After Working Memory Training Dietsje D. Jolles,1,2,3* Mark A. van Buchem,1,3 Eveline A. Crone,1,2 and Serge A.R.B. Rombouts1,2,3 1Leiden Institute for Brain and Cognition (LIBC), Leiden University, P.O. Box 9600, 2300 RC Leiden, The Netherlands 2Institute of Psychology, Leiden University, Wassenaarseweg 52, 2333 AK Leiden, The Netherlands 3Department of Radiology, Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands r r Abstract: Networks of functional connectivity are highly consistent across participants, suggesting that functional connectivity is for a large part predetermined. However, several studies have shown that functional connectivity may change depending on instructions or previous experience. In the present study, we investigated whether 6 weeks of practice with a working memory task changes functional connectivity during a resting period preceding the task. We focused on two task-relevant networks, the frontoparietal network and the default network, using seed regions in the right middle frontal gyrus (MFG) and the medial prefrontal cortex (PFC), respectively. After practice, young adults showed increased functional connectivity between the right MFG and other regions of the frontoparietal net- work, including bilateral superior frontal gyrus, paracingulate gyrus, and anterior cingulate cortex. In addition, they showed reduced functional connectivity between the medial PFC and right posterior middle temporal gyrus. Moreover, a regression with performance changes revealed a positive relation between performance increases and changes of frontoparietal connectivity, and a negative relation between performance increases and changes of default network connectivity. Next, to study whether experience-dependent effects would be different during development, we also examined practice effects in a pilot sample of 12-year-old children. No practice effects were found in this group, suggest- ing that practice-related changes of functional connectivity are age-dependent. Nevertheless, future studies with larger samples are necessary to confirm this hypothesis. Hum Brain Mapp 00:000–000, 2011. VC 2011 Wiley Periodicals, Inc. Key words: resting state; functional connectivity; fMRI; practice; plasticity; development r r Additional Supporting Information may be found in the online Received for publication 24 February 2011; Revised 27 June 2011; version of this article. Accepted 27 July 2011 Contract grant sponsor: S.A.R.B.R. and E.A.C are supported by DOI: 10.1002/hbm.21444 grants from the Netherlands Organization for Scientific Research Published online in Wiley Online Library (wileyonlinelibrary. (NWO, VIDI); Contract grant number: 9178636845207011; Contract com). grant sponsor: Gratama stichting and Leids Universiteits Fonds (granted to E.A.C.). *Correspondence to: Dietsje Jolles, Department of Radiology, Lei- den University Medical Center, P.O. Box 9600, 2300 RC Leiden, The Netherlands. E-mail: [email protected] VC 2011 Wiley Periodicals, Inc. r Jolles et al. r INTRODUCTION 2001]. Third, it has been suggested that repeated coactiva- tion of regions could lead to the Hebbian strengthening of It is well known that brain function depends on large- the functional connections between them [e.g., Fair et al., scale network interactions of brain regions [Mesulam, 2007; Fox and Raichle, 2007; Kelly et al., 2009], suggesting 1998]. Such interactions can be studied with functional that extensive practice with a working memory task could magnetic resonance imaging (fMRI) by analyzing temporal lead to the strengthening of frontoparietal connectivity on correlations of (spontaneous) blood-oxygen level-depend- a more permanent basis. Here, we were specifically inter- ent (BOLD) signal fluctuations between brain regions [Fox ested in those changes of functional connectivity that and Raichle, 2007]. It has been demonstrated that brain extended beyond the context of the task (i.e., the second regions with a similar functionality show a strong tempo- and third possibility). Thus, the main question of the pres- ral correlation, or ‘‘functional connectivity,’’ even in a task- ent study was whether practice with a working memory free setting [Biswal et al., 2010; Smith et al., 2009]. For task affects functional connectivity during resting state. example, strong functional connectivity has been found A secondary goal of the present study was to examine within visual, auditory, and sensorimotor systems, the so- whether experience-dependent effects of functional con- called ‘‘default network,’’ and between brain regions asso- nectivity would also be observed in (a pilot sample of) 12- ciated with higher cognitive functions [Damoiseaux et al., year-old children and whether there would be differences 2006; Smith et al., 2009]. These networks of functional con- between children and adults. Working memory functions, nectivity are highly consistent across participants [Damoi- and related neural activity, improve until late adolescence seaux et al., 2006], suggesting that functional connectivity [Crone et al., 2006; Klingberg et al., 2002; Kwon et al., is for a large part predetermined. 2002; Olesen et al., 2007; Scherf et al., 2006]. This is poten- Other studies, however, have argued that functional tially related to the late maturation of the frontal and pari- connectivity patterns differ between different contexts, etal regions that are involved in working memory [e.g., depending on the instructions that are given [e.g., Benja- Diamond, 2002]. However, in a recent study, we showed min et al., 2010]. Moreover, it has been demonstrated that that children at the age of 12 were able to show a more functional connectivity at rest may predict individual dif- adult-like frontoparietal activation pattern after extensive ferences in behavior [Hampson et al., 2006, 2010; Kelly training (Jolles et al., submitted). Here, we examined et al., 2008; Seeley et al., 2007], and that it can be modified whether children also show changes in resting-state func- as a result of extensive perceptual or motor training tional connectivity after training, and we investigated how [Lewis et al., 2009; Voss et al., 2010]. The goal of the pres- these changes compared with the changes observed in ent study was to examine whether experience-dependent adults. On the one hand, we expected that practice effects changes of functional connectivity could also be observed would be stronger in adults because they might require after training of working memory. advanced cognitive and/or structural brain development. Working memory, or the ability to temporarily store or On the other hand, it could be that activity-dependent manipulate information, is crucial for complex cognitive plasticity is actually stronger during development, when tasks such as reasoning, problem solving, or learning [Bad- functional networks are not yet fully specialized [e.g., Dos- deley, 1992, 2003], and it has often been described as a enbach et al., 2010; Fair et al., 2009; Jolles et al., 2011; Kelly driving force behind the development of cognitive control et al., 2009; Littow et al., 2010; Supekar et al., 2009]. [Case, 1992; Hitch, 2002; Pascual-Leone, 1995]. Several To test these hypotheses, we conducted two experi- studies have shown that practice with a working memory ments. In the first experiment, we examined the effects of task improves performance and modifies activation in the working memory training on resting-state functional con- underlying frontoparietal network [Dahlin et al., 2008; nectivity in young adults. By using a seed-based correla- Jolles et al., 2010; Olesen et al., 2004; Sayala et al., 2006]. tion approach, we focused on two networks involved in Different explanations for the observed practice effects the task: the frontoparietal network, which showed activa- have been suggested [e.g., Kelly and Garavan, 2005], tion during the working memory task [e.g., Jolles et al., including strategy changes taking place on a trial-by-trial 2010], and the default network [Buckner et al., 2008; basis, a general change of approach (e.g., changes of atten- Raichle et al., 2001], which showed deactivation during the tion or task preparation processes), and/or plastic changes task [e.g., Jolles et al., 2010]. The second experiment in the underlying neural network. involved a pilot study that examined the effects of practice Working memory training might also affect the func- in children and compared practice effects between chil- tional connectivity between the regions that are involved dren and adults. in the task. First, a strategy change might not only lead to differential contributions of particular regions but also to a change in their interactions. Second, task preparation proc- MATERIALS AND METHODS esses could change the coordination of information flow Participants through the brain, which may influence functional connec- ¼ ¼ tivity already before start of the task [Buzsaki and Dra- Fifteen adults [Mage 22.04 years (SD 1.85) and eight ¼ ¼ guhn, 2004; Fox and Raichle, 2007; Salinas and Sejnowski, female] and nine children [Mage 12.24 years (SD 0.61) r 2 r r Training and Functional Connectivity r and five female] were included in the analyses. Data from sequences of four objects, and one block with sequences of two other children were excluded due to scanner artifacts five objects. On average, the children practiced 15 times and because one child got engaged in an accident in (SD ¼ 2.76) during the 6-week period, and the adults prac- between the scanning sessions. A chi-square analysis con- ticed 16 times (SD ¼ 1.73). The number of practice sessions firmed that the sex distribution did not differ between age did not differ significantly between groups [F(1,22) ¼ 3.00 groups [v2(1, N ¼ 24) ¼ 0.11 and P ¼ 0.92]. All partici- and P ¼ 0.10]. The working memory task that was used pants gave written informed consent for participation in during scanning sessions was the same as the task that the study. Parents of children that participated in the was used for practice, except that different pictures were study gave written informed consent as well.
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