The role of fronto-parietal and fronto-striatal networks in the development of working memory: a longitudinal study.

The increase in working memory (WM) capacity is an important part of cognitive development during childhood and adolescence. Cross-sectional analyses have associated this development with higher activity, thinner cortex, and white matter maturation in fronto-parietal networks. However, there is still a lack of longitudinal data showing the dynamics of this development and the role of subcortical structures. We included 89 individuals, aged 6-25 years, who were scanned 1-3 times at 2-year intervals. Functional magnetic resonance imaging (fMRI) was used to identify activated areas in superior frontal, intraparietal cortices, and caudate nucleus during performance on a visuo-spatial WM task. Probabilistic tractography determined the anatomical pathways between these regions. In the cross-sectional analysis, WM capacity correlated with activity in frontal and parietal regions, cortical thickness in parietal cortex, and white matter structure [both fractional anisotropy (FA) and white matter volume] of fronto-parietal and fronto-striatal tracts. However, in the longitudinal analysis, FA in white matter tracts and activity in caudate predicted future WM capacity. The results show a dynamic of neural networks underlying WM development in which cortical activity and structure relate to current capacity, while white matter tracts and caudate activity predict future WM capacity.

[1]  B. Postle,et al.  Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. , 2000, Brain research. Brain research protocols.

[2]  Anders M. Dale,et al.  Longitudinal Working Memory Development Is Related to Structural Maturation of Frontal and Parietal Cortices , 2013, Journal of Cognitive Neuroscience.

[3]  Lars Bäckman,et al.  Transfer of Learning After Updating Training Mediated by the Striatum , 2008, Science.

[4]  K. Walhovd,et al.  Morphometry and connectivity of the fronto-parietal verbal working memory network in development , 2011, Neuropsychologia.

[5]  Heidi Johansen-Berg,et al.  Unconscious vision: new insights into the neuronal correlate of blindsight using diffusion tractography. , 2006, Brain : a journal of neurology.

[6]  G. Bush,et al.  Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. , 2007, Cerebral cortex.

[7]  Daniel Fürth,et al.  Working memory plasticity modulated by dopamine transporter genotype , 2009, Neuroscience Letters.

[8]  T. Klingberg,et al.  Maturation of White Matter is Associated with the Development of Cognitive Functions during Childhood , 2004, Journal of Cognitive Neuroscience.

[9]  A. Graybiel.  Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[10]  L. Westlye,et al.  Neuroanatomical correlates of executive functions in children and adolescents: A magnetic resonance imaging (MRI) study of cortical thickness , 2010, Neuropsychologia.

[11]  G J Hitch,et al.  Working memory impairments in children with specific arithmetic learning difficulties. , 1999, Journal of experimental child psychology.

[12]  T. Klingberg.  Training and plasticity of working memory , 2010, Trends in Cognitive Sciences.

[13]  Torkel Klingberg,et al.  Polymorphisms in the Dopamine Receptor 2 Gene Region Influence Improvements during Working Memory Training in Children and Adolescents , 2014, Journal of Cognitive Neuroscience.

[14]  Carter Wendelken,et al.  Neurocognitive development of the ability to manipulate information in working memory. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Iroise Dumontheil,et al.  Influence of the COMT Genotype on Working Memory and Brain Activity Changes During Development , 2011, Biological Psychiatry.

[16]  Alan C. Evans,et al.  Intellectual ability and cortical development in children and adolescents , 2006, Nature.

[17]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  S. Hogg-Johnson,et al.  A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[19]  Yasuyuki Taki,et al.  Verbal working memory performance correlates with regional white matter structures in the frontoparietal regions , 2011, Neuropsychologia.

[20]  Nikos Makris,et al.  Attention and executive systems abnormalities in adults with childhood ADHD: A DT-MRI study of connections. , 2008, Cerebral cortex.

[21]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[22]  Hans Forssberg,et al.  Visuo-Spatial Working Memory Span: A Sensitive Measure of Cognitive Deficits in Children With ADHD , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[23]  Susan E. Gathercole,et al.  Working memory assessments at school entry as longitudinal predictors of National Curriculum attainment levels , 2003, Educational and Child Psychology.

[24]  Irene E. Nagel,et al.  Microstructure of frontoparietal connections predicts cortical responsivity and working memory performance. , 2011, Cerebral cortex.

[25]  Matti Laine,et al.  Effects of Working-Memory Training on Striatal Dopamine Release , 2011, Science.

[26]  J. Kere,et al.  The SNAP25 Gene Is Linked to Working Memory Capacity and Maturation of the Posterior Cingulate Cortex During Childhood , 2010, Biological Psychiatry.

[27]  Kirstie J. Whitaker,et al.  Increased Functional Selectivity over Development in Rostrolateral Prefrontal Cortex , 2011, The Journal of Neuroscience.

[28]  J. Kere,et al.  Dopamine, working memory, and training induced plasticity: implications for developmental research. , 2012, Developmental psychology.

[29]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[30]  T. Klingberg,et al.  Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. , 2003, Brain research. Cognitive brain research.

[31]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[32]  Olaf B. Paulson,et al.  White Matter Microstructure in Superior Longitudinal Fasciculus Associated with Spatial Working Memory Performance in Children , 2011, Journal of Cognitive Neuroscience.

[33]  Yasuyuki Taki,et al.  Associations among imaging measures (2): The association between gray matter concentration and task‐induced activation changes , 2014, Human brain mapping.

[34]  Valérie Camos,et al.  Low working memory capacity impedes both efficiency and learning of number transcoding in children. , 2008, Journal of experimental child psychology.

[35]  T Klingberg,et al.  Working memory brain activity and capacity link MAOA polymorphism to aggressive behavior during development , 2012, Translational Psychiatry.

[36]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

[37]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[38]  P. Goldman-Rakic,et al.  Differential Activation of the Caudate Nucleus in Primates Performing Spatial and Nonspatial Working Memory Tasks , 1997, The Journal of Neuroscience.

[39]  Beatriz Luna,et al.  Brain Basis of Developmental Change in Visuospatial Working Memory , 2006, Journal of Cognitive Neuroscience.

[40]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[41]  J. Ware,et al.  Applied Longitudinal Analysis , 2004 .

[42]  Bruce Fischl,et al.  Avoiding asymmetry-induced bias in longitudinal image processing , 2011, NeuroImage.

[43]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[44]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[45]  T. Klingberg,et al.  Increased prefrontal and parietal activity after training of working memory , 2004, Nature Neuroscience.

[46]  H. Forssberg,et al.  Computerized training of working memory in children with ADHD--a randomized, controlled trial. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[47]  Zeynep M. Saygin,et al.  Anatomical connectivity patterns predict face-selectivity in the fusiform gyrus , 2011, Nature Neuroscience.

[48]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[49]  Torkel Klingberg,et al.  Structural Maturation and Brain Activity Predict Future Working Memory Capacity during Childhood Development , 2014, The Journal of Neuroscience.

[50]  Amy Devine,et al.  Developmental dyscalculia is related to visuo-spatial memory and inhibition impairment☆ , 2013, Cortex.

[51]  A. Graybiel,et al.  Temporal and spatial characteristics of tonically active neurons of the primate's striatum. , 1995, Journal of neurophysiology.

[52]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Nigg,et al.  Is ADHD a disinhibitory disorder? , 2001, Psychological bulletin.

[54]  L. Westlye,et al.  The brain dynamics of intellectual development: Waxing and waning white and gray matter , 2011, Neuropsychologia.

[55]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[56]  Iroise Dumontheil,et al.  Brain activity during a visuospatial working memory task predicts arithmetical performance 2 years later. , 2012, Cerebral cortex.

[57]  T. Klingberg.  Development of a superior frontal–intraparietal network for visuo-spatial working memory , 2006, Neuropsychologia.

[58]  Jesper Tegnér,et al.  Brain activity related to working memory and distraction in children and adults. , 2006, Cerebral cortex.

[59]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.