White matter structure and myelin-related gene expression alterations with experience in adult rats

Highlights • Somatosensory experience results in DTI changes in white matter (WM).• Macroscale metrics of WM structure correlate with mRNA markers of cortical activity.• MBP immunohistochemistry and mRNA expression indicate changes in myelin.• Both molecular and cellular evidence are consistent with DTI findings.• Myelination is one component of macroscale measures of WM plasticity.

[1]  J. Testa,et al.  Perturbations of the AKT signaling pathway in human cancer , 2005, Oncogene.

[2]  Marc Montminy,et al.  Transcriptional regulation by the phosphorylation-dependent factor CREB , 2001, Nature Reviews Molecular Cell Biology.

[3]  E. Welker,et al.  Upregulation of BDNF mRNA Expression in the Barrel Cortex of Adult Mice after Sensory Stimulation , 1996, The Journal of Neuroscience.

[4]  William D. Richardson,et al.  Motor skill learning requires active central myelination , 2014, Science.

[5]  W. Macklin,et al.  Interaction of mTOR and Erk1/2 signaling to regulate oligodendrocyte differentiation , 2014, Glia.

[6]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[7]  Christopher M. Taylor,et al.  Proteomic mapping provides powerful insights into functional myelin biology. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[8]  G. Almazan,et al.  IGF‐I‐induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src‐like tyrosine kinases , 2007, Journal of neurochemistry.

[9]  Huitu Liu,et al.  MAPK signal pathways in the regulation of cell proliferation in mammalian cells , 2002, Cell Research.

[10]  G. Knott,et al.  Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice , 2002, Neuron.

[11]  D. G. Herrera,et al.  Activation of c-fos in the brain , 1996, Progress in Neurobiology.

[12]  D. Meffre,et al.  Lithium chloride stimulates PLP and MBP expression in oligodendrocytes via Wnt/β-catenin and Akt/CREB pathways , 2015, Neuroscience.

[13]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[14]  D. Attwell,et al.  Node of Ranvier length as a potential regulator of myelinated axon conduction speed , 2017, eLife.

[15]  Christopher W Mount,et al.  Neuronal Activity Promotes Oligodendrogenesis and Adaptive Myelination in the Mammalian Brain , 2014, Science.

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

[17]  Y. Assaf,et al.  Diffusion MRI of Structural Brain Plasticity Induced by a Learning and Memory Task , 2011, PloS one.

[18]  S. Tenzer,et al.  Systematic approaches to central nervous system myelin , 2012, Cellular and Molecular Life Sciences.

[19]  D. Bergles,et al.  Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex , 2018, Nature Neuroscience.

[20]  A. Ishii,et al.  Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation , 2012, Glia.

[21]  A. El Manira,et al.  Synaptic vesicle release regulates the number of myelin sheaths made by individual oligodendrocytes in vivo , 2015, Nature Neuroscience.

[22]  Alex J. de Crespigny,et al.  An approach to high resolution diffusion tensor imaging in fixed primate brain , 2007, NeuroImage.

[23]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[24]  Thomas E. Nichols,et al.  Non‐parametric combination and related permutation tests for neuroimaging , 2016, Human brain mapping.

[25]  Yaniv Assaf,et al.  Short-Term Learning Induces White Matter Plasticity in the Fornix , 2013, The Journal of Neuroscience.

[26]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[27]  U. Suter,et al.  Akt/mTOR signalling in myelination. , 2013, Biochemical Society transactions.

[28]  A. Barco,et al.  CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models , 2010, Trends in Neurosciences.

[29]  J. Helpern,et al.  Diffusion tensor imaging in fixed brain tissue at 7.0 T , 2003, NMR in biomedicine.

[30]  T. Zhao,et al.  Translational Control of Myelin Basic Protein Expression by ERK2 MAP Kinase Regulates Timely Remyelination in the Adult Brain , 2015, The Journal of Neuroscience.

[31]  G. Wegener,et al.  Reference genes for normalization: A study of rat brain tissue , 2008, Synapse.

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

[33]  C. Der,et al.  Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer , 2007, Oncogene.

[34]  Brad T. Sherman,et al.  Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists , 2008, Nucleic acids research.

[35]  Karel Svoboda,et al.  Structural Plasticity within the Barrel Cortex during Initial Phases of Whisker-Dependent Learning , 2014, The Journal of Neuroscience.

[36]  Heidi Johansen-Berg,et al.  Motor Skill Learning Induces Changes in White Matter Microstructure and Myelination , 2013, The Journal of Neuroscience.

[37]  W. Richardson,et al.  Rapid production of new oligodendrocytes is required in the earliest stages of motor skill learning , 2016, Nature Neuroscience.

[38]  Laura R. Fenlon,et al.  Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner , 2018, Nature Communications.

[39]  H. Johansen-Berg,et al.  White Matter Plasticity in the Adult Brain , 2017, Neuron.

[40]  B. Spann,et al.  Transcriptome Analysis of Synaptoneurosomes Identifies Neuroplasticity Genes Overexpressed in Incipient Alzheimer's Disease , 2009, PloS one.

[41]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[42]  K. Nave,et al.  Myelin Membrane Wrapping of CNS Axons by PI(3,4,5)P3-Dependent Polarized Growth at the Inner Tongue , 2014, Cell.

[43]  P. Basser,et al.  Regulation of myelin structure and conduction velocity by perinodal astrocytes , 2018, Proceedings of the National Academy of Sciences.

[44]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[45]  Brad T. Sherman,et al.  DAVID: Database for Annotation, Visualization, and Integrated Discovery , 2003, Genome Biology.

[46]  Y. Tesfaigzi,et al.  How ERK1/2 activation controls cell proliferation and cell death: Is subcellular localization the answer? , 2009, Cell cycle.

[47]  Denise M. Piscopo,et al.  Changes in white matter in mice resulting from low-frequency brain stimulation , 2018, Proceedings of the National Academy of Sciences.

[48]  A. Ishii,et al.  ERK1/ERK2 MAPK Signaling is Required to Increase Myelin Thickness Independent of Oligodendrocyte Differentiation and Initiation of Myelination , 2012, The Journal of Neuroscience.

[49]  D. Ginty,et al.  Function and Regulation of CREB Family Transcription Factors in the Nervous System , 2002, Neuron.

[50]  James L. Sinclair,et al.  Sound-Evoked Activity Influences Myelination of Brainstem Axons in the Trapezoid Body , 2017, The Journal of Neuroscience.

[51]  M. Rubio,et al.  ERK1/2 Activation in Preexisting Oligodendrocytes of Adult Mice Drives New Myelin Synthesis and Enhanced CNS Function , 2016, The Journal of Neuroscience.

[52]  M. Diamond,et al.  Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination , 2007, PLoS biology.

[53]  Sheng-Kwei Song,et al.  Relative indices of water diffusion anisotropy are equivalent in live and formalin‐fixed mouse brains , 2003, Magnetic resonance in medicine.

[54]  Olivia Bibollet-Bahena,et al.  IGF‐1‐stimulated protein synthesis in oligodendrocyte progenitors requires PI3K/mTOR/Akt and MEK/ERK pathways , 2009, Journal of neurochemistry.

[55]  A. Blight,et al.  Dalfampridine: a brief review of its mechanism of action and efficacy as a treatment to improve walking in patients with multiple sclerosis , 2011, Current medical research and opinion.

[56]  E. Ullian,et al.  Dynamic Modulation of Myelination in Response to Visual Stimuli Alters Optic Nerve Conduction Velocity , 2016, The Journal of Neuroscience.

[57]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[58]  F. Helmchen,et al.  Barrel cortex function , 2013, Progress in Neurobiology.

[59]  B. Stankoff,et al.  Induction of myelination in the central nervous system by electrical activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Increased Synaptophysin Expression Through Whisker Stimulation in Rat , 2002, Cellular and Molecular Neurobiology.

[61]  Karel Svoboda,et al.  Experience-dependent and cell-type-specific spine growth in the neocortex , 2006, Nature.

[62]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[63]  Arno Villringer,et al.  Dynamic Properties of Human Brain Structure: Learning-Related Changes in Cortical Areas and Associated Fiber Connections , 2010, The Journal of Neuroscience.

[64]  Marcin Szwed,et al.  Functional and Structural Neuroplasticity Induced by Short-Term Tactile Training Based on Braille Reading , 2016, Front. Neurosci..

[65]  M. Noble,et al.  4‐Aminopyridine promotes functional recovery and remyelination in acute peripheral nerve injury , 2016, EMBO molecular medicine.