Working memory training impacts the mean diffusivity in the dopaminergic system

Dopaminergic transmission plays a critical role in working memory (WM). Mean diffusivity (MD) is a sensitive and unique neuroimaging tool for detecting microstructural differences particularly in the areas of the dopaminergic system. Despite previous investigation of the effects of WM training (WMT) on dopamine receptor binding potentials, the effects of WMT on MD remain unknown. In this study, we investigated these effects in young adult subjects who either underwent WMT or received no intervention for 4 weeks. Before and after the intervention or no-intervention periods, subjects underwent scanning sessions in diffusion-weighted imaging to measure MD. Compared with no intervention, WMT resulted in an increase in MD in the bilateral caudate, right putamen, left dorsolateral prefrontal cortex (DLPFC), right anterior cingulate cortex (ACC), right substantia nigra, and ventral tegmental area. Furthermore, the increase in performance on WMT tasks was significantly positively correlated with the mean increase in MD in the clusters of the left DLPFC and of the right ACC. These results suggest that WMT caused microstructural changes in the regions of the dopaminergic system in a way that is usually interpreted as a reduction in neural components.

[1]  Yasuyuki Taki,et al.  Effects of Training of Processing Speed on Neural Systems , 2011, The Journal of Neuroscience.

[2]  C. J. McGrath,et al.  Effect of exchange rate return on volatility spill-over across trading regions , 2012 .

[3]  Gregory McCarthy,et al.  Enhanced Spatial Localization of Neuronal Activation Using Simultaneous Apparent-Diffusion-Coefficient and Blood-Oxygenation Functional Magnetic Resonance Imaging , 2002, NeuroImage.

[4]  Yoshiro Okubo,et al.  Dopamine D2 Receptors in the Insular Cortex and the Personality Trait of Novelty Seeking , 2001, NeuroImage.

[5]  Susanne M. Jaeggi,et al.  Improving fluid intelligence with training on working memory: a meta-analysis , 2008, Psychonomic Bulletin & Review.

[6]  Yasuyuki Taki,et al.  Cerebral Blood Flow during Rest Associates with General Intelligence and Creativity , 2011, PloS one.

[7]  N. Carlson.  Physiology of behavior , 1977 .

[8]  Tao Jin,et al.  Functional changes of apparent diffusion coefficient during visual stimulation investigated by diffusion-weighted gradient-echo fMRI , 2008, NeuroImage.

[9]  Yasuyuki Taki,et al.  Training of Working Memory Impacts Structural Connectivity , 2010, The Journal of Neuroscience.

[10]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[11]  H. Forssberg,et al.  Changes in Cortical Dopamine D1 Receptor Binding Associated with Cognitive Training , 2009, NeuroImage.

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

[13]  R. Kawashima,et al.  Regional gray matter density is associated with achievement motivation: evidence from voxel-based morphometry , 2012, Brain Structure and Function.

[14]  Hidenao Fukuyama,et al.  Water diffusion reveals networks that modulate multiregional morphological plasticity after repetitive brain stimulation , 2014, Proceedings of the National Academy of Sciences.

[15]  R. Kawashima,et al.  Regional Gray Matter Volume Is Associated with Empathizing and Systemizing in Young Adults , 2014, PloS one.

[16]  Heidi Johansen-Berg,et al.  Human Structural Plasticity at Record Speed , 2012, Neuron.

[17]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[18]  B. Ames,et al.  An overview of evidence for a causal relation between iron deficiency during development and deficits in cognitive or behavioral function. , 2007, The American journal of clinical nutrition.

[19]  D. Dimitrov,et al.  Pretest-posttest designs and measurement of change. , 2003, Work.

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

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

[22]  Pierre-Yves Oudeyer,et al.  In Search of the Neural Circuits of Intrinsic Motivation , 2007, Front. Neurosci..

[23]  Thomas E. Nichols,et al.  Validating cluster size inference: random field and permutation methods , 2003, NeuroImage.

[24]  Kjell Någren,et al.  Insular dopamine D2 receptors and novelty seeking personality in Parkinson's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[25]  W. Jagust,et al.  Striatal dopamine and working memory. , 2009, Cerebral cortex.

[26]  Peter Cloetens,et al.  Iron Storage within Dopamine Neurovesicles Revealed by Chemical Nano-Imaging , 2007, PloS one.

[27]  Yasuyuki Taki,et al.  Effects of working memory training on functional connectivity and cerebral blood flow during rest , 2013, Cortex.

[28]  Chris I. Baker,et al.  Teaching an adult brain new tricks: A critical review of evidence for training-dependent structural plasticity in humans , 2013, NeuroImage.

[29]  Matti Laine,et al.  Frontal and Temporal Dopamine Release during Working Memory and Attention Tasks in Healthy Humans: a Positron Emission Tomography Study Using the High-Affinity Dopamine D2 Receptor Ligand [11C]FLB 457 , 2005, The Journal of Neuroscience.

[30]  C Barbui,et al.  Cortical white-matter microstructure in schizophrenia. Diffusion imaging study. , 2007, The British journal of psychiatry : the journal of mental science.

[31]  Dardo Tomasi,et al.  Functional connectivity of substantia nigra and ventral tegmental area: maturation during adolescence and effects of ADHD. , 2014, Cerebral cortex.

[32]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[33]  Werner Jaschke,et al.  Comparison of diffusion‐weighted imaging and [123I]IBZM‐SPECT for the differentiation of patients with the Parkinson variant of multiple system atrophy from those with Parkinson's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[34]  Veronique D. Bohbot,et al.  Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning , 2011, NeuroImage.

[35]  S R Lord,et al.  The effect of group-based exercise on cognitive performance and mood in seniors residing in intermediate care and self-care retirement facilities: a randomised controlled trial , 2008, British Journal of Sports Medicine.

[36]  A. Baddeley.  Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

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

[38]  Ahmed Abdel Khalek Abdel Razek,et al.  Idiopathic Parkinson disease effect of levodopa on apparent diffusion coefficient value of the brain. , 2011, Academic radiology.

[39]  Yaniv Assaf,et al.  Learning in the Fast Lane: New Insights into Neuroplasticity , 2012, Neuron.

[40]  Yasuyuki Taki,et al.  Effects of Working Memory Training on Cognitive Functions and Neural Systems , 2010, Reviews in the neurosciences.

[41]  Benjamin Thyreau,et al.  White matter structures associated with empathizing and systemizing in young adults , 2013, NeuroImage.

[42]  R. V. Van Heertum,et al.  Prefrontal Dopamine D1 Receptors and Working Memory in Schizophrenia , 2002, The Journal of Neuroscience.

[43]  R Zemke,et al.  Occupational therapy for independent-living older adults. A randomized controlled trial. , 1997, JAMA.

[44]  Jianju Liu,et al.  Regional diffusion changes of cerebral grey matter during normal aging--a fluid-inversion prepared diffusion imaging study. , 2010, European journal of radiology.

[45]  F. Crawford,et al.  DRD4 and novelty seeking: results of meta-analyses. , 2002, American journal of medical genetics.

[46]  Lauren E. Milton,et al.  Annual Meeting—President's Address , 1945 .

[47]  M. Gluck,et al.  Reward-learning and the novelty-seeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinson's patients. , 2009, Brain : a journal of neurology.

[48]  B. Gandevia,et al.  DECLARATION OF HELSINKI. , 1964, The Medical journal of Australia.

[49]  W. Hauber,et al.  Dopamine D1 receptors in the anterior cingulate cortex regulate effort-based decision making. , 2006, Learning & memory.

[50]  C. Jack,et al.  Mild cognitive impairment and Alzheimer disease: regional diffusivity of water. , 2001, Radiology.

[51]  Yasuyuki Taki,et al.  Working Memory Training Using Mental Calculation Impacts Regional Gray Matter of the Frontal and Parietal Regions , 2011, PloS one.

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

[53]  A. Stefani,et al.  Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. , 2010, Brain : a journal of neurology.

[54]  M S Buchsbaum,et al.  Regional and global changes in cerebral diffusion with normal aging. , 2001, AJNR. American journal of neuroradiology.

[55]  Sharona M. Atkins,et al.  Memory enhancement in healthy older adults using a brain plasticity-based training program: A randomized, controlled study , 2006, Proceedings of the National Academy of Sciences.

[56]  Yasuyuki Taki,et al.  Failing to deactivate: The association between brain activity during a working memory task and creativity , 2011, NeuroImage.

[57]  Ramon Casanova,et al.  Biological parametric mapping: A statistical toolbox for multimodality brain image analysis , 2007, NeuroImage.

[58]  R. Sener,et al.  Echo-planar and gradient-echo diffusion MRI of normal brain iron in the globus pallidus. , 2002, Clinical imaging.

[59]  J. Aharon-Peretz,et al.  Novelty seeking and harm avoidance in Parkinson’s disease: effects of asymmetric dopamine deficiency , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[60]  Monica Melby-Lervåg,et al.  Is working memory training effective? A meta-analytic review. , 2013, Developmental psychology.

[61]  J. Illes,et al.  Diffusion-tensor imaging of cognitive performance , 2002, Brain and Cognition.

[62]  Yasuyuki Taki,et al.  Effects of multitasking‐training on gray matter structure and resting state neural mechanisms , 2013, Human brain mapping.