Plasticity in gray and white: neuroimaging changes in brain structure during learning (original) (raw)

• He, Y., Chen, Z.J. & Evans, A.C. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb. Cortex 17, 2407–2419 (2007).
  PubMed Google Scholar
• Raznahan, A. et al. Patterns of coordinated anatomical change in human cortical development: a longitudinal neuroimaging study of maturational coupling. Neuron 72, 873–884 (2011).
  CAS PubMed PubMed Central Google Scholar
• Bermudez, P., Evans, A.C., Lerch, J.P. & Zatorre, R.J. Neuro-anatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. Cereb. Cortex 19, 1583–1596 (2009).
  PubMed Google Scholar
• Maguire, E.A. et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. USA 97, 4398–4403 (2000).
  CAS PubMed PubMed Central Google Scholar
• Schneider, P. et al. Morphology of Heschl's gyrus reflects enhanced activation in the auditory cortex of musicians. Nat. Neurosci. 5, 688–694 (2002).
  CAS PubMed Google Scholar
• Bengtsson, S.L. et al. Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 8, 1148–1150 (2005).
  CAS PubMed Google Scholar
• Draganski, B. et al. Neuroplasticity: changes in grey matter induced by training. Nature 427, 311–312 (2004).
  CAS PubMed Google Scholar
• Driemeyer, J., Boyke, J., Gaser, C., Buchel, C. & May, A. Changes in gray matter induced by learning–revisited. PLoS ONE 3, e2669 (2008).
  PubMed PubMed Central Google Scholar
• Scholz, J., Klein, M.C., Behrens, T.E. & Johansen-Berg, H. Training induces changes in white-matter architecture. Nat. Neurosci. 12, 1370–1371 (2009).
  CAS PubMed PubMed Central Google Scholar
• Taubert, M. et al. Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J. Neurosci. 30, 11670–11677 (2010).
  CAS PubMed PubMed Central Google Scholar
• Takeuchi, H. et al. Training of working memory impacts structural connectivity. J. Neurosci. 30, 3297–3303 (2010).
  CAS PubMed PubMed Central Google Scholar
• Thompson, P.M. et al. Genetic influences on brain structure. Nat. Neurosci. 4, 1253–1258 (2001).
  CAS PubMed Google Scholar
• Chiang, M.C. et al. Genetics of brain fiber architecture and intellectual performance. J. Neurosci. 29, 2212–2224 (2009).
  CAS PubMed PubMed Central Google Scholar
• Golestani, N., Molko, N., Dehaene, S., LeBihan, D. & Pallier, C. Brain structure predicts the learning of foreign speech sounds. Cereb. Cortex 17, 575–582 (2007).
  PubMed Google Scholar
• Wong, P.C. et al. Volume of left Heschl's gyrus and linguistic pitch learning. Cereb. Cortex 18, 828–836 (2008).
  PubMed Google Scholar
• Foster, N.E. & Zatorre, R.J. Cortical structure predicts success in performing musical transformation judgments. Neuroimage 53, 26–36 (2010).
  PubMed Google Scholar
• Laule, C. et al. Myelin water imaging in multiple sclerosis: quantitative correlations with histopathology. Mult. Scler. 12, 747–753 (2006).
  CAS PubMed Google Scholar
• Beaulieu, C. The biological basis of diffusion anisotropy. in Diffusion MRI: From Quantitative Measurement to In-Vivo Neuroanatomy (eds. Johansen-Berg, H. & Behrens, T.E.J.) 105–126 (Elsevier, London, 2009).
• Wedeen, V.J., Hagmann, P., Tseng, W.Y., Reese, T.G. & Weisskoff, R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 54, 1377–1386 (2005).
  PubMed Google Scholar
• Lerch, J.P. et al. Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage 54, 2086–2095 (2011).
  PubMed Google Scholar
• Barbier, E.L., Lamalle, L. & Decorps, M. Methodology of brain perfusion imaging. J. Magn. Reson. Imaging 13, 496–520 (2001).
  CAS PubMed Google Scholar
• Tronel, S. et al. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc. Natl. Acad. Sci. USA 107, 7963–7968 (2010).
  CAS PubMed PubMed Central Google Scholar
• Deng, W., Saxe, M.D., Gallina, I.S. & Gage, F.H. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J. Neurosci. 29, 13532–13542 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sahay, A. et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466–470 (2011).
  CAS PubMed PubMed Central Google Scholar
• Aimone, J.B., Wiles, J. & Gage, F.H. Computational influence of adult neurogenesis on memory encoding. Neuron 61, 187–202 (2009).
  CAS PubMed PubMed Central Google Scholar
• Gould, E., Reeves, A.J., Graziano, M.S. & Gross, C.G. Neurogenesis in the neocortex of adult primates. Science 286, 548–552 (1999).
  CAS PubMed Google Scholar
• Iordanova, B. & Ahrens, E.T. In vivo magnetic resonance imaging of ferritin-based reporter visualizes native neuroblast migration. Neuroimage 59, 1004–1012 (2011).
  PubMed Google Scholar
• Nieman, B.J. et al. In vivo MRI of neural cell migration dynamics in the mouse brain. Neuroimage 50, 456–464 (2010).
  PubMed Google Scholar
• Rakic, P. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat. Rev. Neurosci. 3, 65–71 (2002).
  CAS PubMed Google Scholar
• Dong, W.K. & Greenough, W.T. Plasticity of nonneuronal brain tissue: roles in developmental disorders. Ment. Retard. Dev. Disabil. Res. Rev. 10, 85–90 (2004).
  PubMed Google Scholar
• Wang, X., Takano, T. & Nedergaard, M. Astrocytic calcium signaling: mechanism and implications for functional brain imaging. Methods Mol. Biol. 489, 93–109 (2009).
  CAS PubMed PubMed Central Google Scholar
• Tremblay, M.È., Lowery, R.L. & Majewska, A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8, e1000527 (2010).
  PubMed PubMed Central Google Scholar
• Wake, H., Moorhouse, A.J., Jinno, S., Kohsaka, S. & Nabekura, J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974–3980 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kleim, J.A. et al. Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem. 77, 63–77 (2002).
  PubMed Google Scholar
• Kolb, B., Cioe, J. & Comeau, W. Contrasting effects of motor and visual spatial learning tasks on dendritic arborization and spine density in rats. Neurobiol. Learn. Mem. 90, 295–300 (2008).
  PubMed Google Scholar
• Kleim, J.A. et al. Motor learning induces astrocytic hypertrophy in the cerebellar cortex. Behav. Brain Res. 178, 244–249 (2007).
  PubMed PubMed Central Google Scholar
• Yang, G., Pan, F. & Gan, W.B. Stably maintained dendritic spines are associated with lifelong memories. Nature 462, 920–924 (2009).
  CAS PubMed PubMed Central Google Scholar
• Draganski, B. et al. Temporal and spatial dynamics of brain structure changes during extensive learning. J. Neurosci. 26, 6314–6317 (2006).
  CAS PubMed PubMed Central Google Scholar
• Rhyu, I.J. et al. Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 167, 1239–1248 (2010).
  CAS PubMed Google Scholar
• Pereira, A.C. et al. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. USA 104, 5638–5643 (2007).
  CAS PubMed PubMed Central Google Scholar
• Klintsova, A.Y., Dickson, E., Yoshida, R. & Greenough, W.T. Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res. 1028, 92–104 (2004).
  CAS PubMed Google Scholar
• Pezawas, L. et al. The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology. J. Neurosci. 24, 10099–10102 (2004).
  CAS PubMed PubMed Central Google Scholar
• Egan, M.F. et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257–269 (2003).
  CAS PubMed Google Scholar
• Cheeran, B. et al. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol. (Lond.) 586, 5717–5725 (2008).
  CAS Google Scholar
• Xiao, J. et al. Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neurosignals 18, 186–202 (2010).
  CAS PubMed Google Scholar
• Cohen, J.E. & Fields, R.D. Activity-dependent neuron-glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development. Neuron Glia Biol. 4, 43–55 (2008).
  PubMed PubMed Central Google Scholar
• Datwani, A. et al. Classical MHCI molecules regulate retinogeniculate refinement and limit ocular dominance plasticity. Neuron 64, 463–470 (2009).
  CAS PubMed PubMed Central Google Scholar
• Stevens, B. et al. The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164–1178 (2007).
  CAS PubMed Google Scholar
• Licht, T. et al. Reversible modulations of neuronal plasticity by VEGF. Proc. Natl. Acad. Sci. USA 108, 5081–5086 (2011).
  CAS PubMed PubMed Central Google Scholar
• Fields, R.D. White matter in learning, cognition and psychiatric disorders. Trends Neurosci. 31, 361–370 (2008).
  CAS PubMed PubMed Central Google Scholar
• Concha, L., Livy, D.J., Beaulieu, C., Wheatley, B.M. & Gross, D.W. In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. J. Neurosci. 30, 996–1002 (2010).
  CAS PubMed PubMed Central Google Scholar
• Takahashi, M. et al. Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord. Proc. Natl. Acad. Sci. USA 99, 16192–16196 (2002).
  CAS PubMed PubMed Central Google Scholar
• Fields, R.D. Neuroscience. Change in the brain's white matter. Science 330, 768–769 (2010).
  CAS PubMed PubMed Central Google Scholar
• Psachoulia, K., Jamen, F., Young, K.M. & Richardson, W.D. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol. 5, 57–67 (2009).
  PubMed PubMed Central Google Scholar
• Peters, A., Verderosa, A. & Sethares, C. The neuroglial population in the primary visual cortex of the aging rhesus monkey. Glia 56, 1151–1161 (2008).
  PubMed Google Scholar
• Ruegg, D.G., Kakebeeke, T.H., Gabriel, J.P. & Bennefeld, M. Conduction velocity of nerve and muscle fiber action potentials after a space mission or a bed rest. Clin. Neurophysiol. 114, 86–93 (2003).
  PubMed Google Scholar
• Canu, M.H., Carnaud, M., Picquet, F. & Goutebroze, L. Activity-dependent regulation of myelin maintenance in the adult rat. Brain Res. 1252, 45–51 (2009).
  CAS PubMed Google Scholar
• Markham, J.A., Herting, M.M., Luszpak, A.E., Juraska, J.M. & Greenough, W.T. Myelination of the corpus callosum in male and female rats following complex environment housing during adulthood. Brain Res. 1288, 9–17 (2009).
  CAS PubMed PubMed Central Google Scholar
• Blumenfeld-Katzir, T., Pasternak, O., Dagan, M. & Assaf, Y. Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS ONE 6, e20678 (2011).
  CAS PubMed PubMed Central Google Scholar
• Adams, B., Lee, M., Fahnestock, M. & Racine, R.J. Long-term potentiation trains induce mossy fiber sprouting. Brain Res. 775, 193–197 (1997).
  CAS PubMed Google Scholar
• Ramírez-Amaya, V., Escobar, M.L., Chao, V. & Bermudez-Rattoni, F. Synaptogenesis of mossy fibers induced by spatial water maze overtraining. Hippocampus 9, 631–636 (1999).
  PubMed Google Scholar
• Toscano-Silva, M. et al. Hippocampal mossy fiber sprouting induced by forced and voluntary physical exercise. Physiol. Behav. 101, 302–308 (2010).
  CAS PubMed Google Scholar
• Yasuda, M. et al. Multiple forms of activity-dependent competition refine hippocampal circuits in vivo. Neuron 70, 1128–1142 (2011).
  CAS PubMed PubMed Central Google Scholar
• Johansen-Berg, H. Structural plasticity: rewiring the brain. Curr. Biol. 17, R141–R144 (2007).
  CAS PubMed Google Scholar
• Dancause, N. et al. Extensive cortical rewiring after brain injury. J. Neurosci. 25, 10167–10179 (2005).
  CAS PubMed PubMed Central Google Scholar
• Kukley, M., Capetillo-Zarate, E. & Dietrich, D. Vesicular glutamate release from axons in white matter. Nat. Neurosci. 10, 311–320 (2007).
  CAS PubMed Google Scholar
• Ziskin, J.L., Nishiyama, A., Rubio, M., Fukaya, M. & Bergles, D.E. Vesicular release of glutamate from unmyelinated axons in white matter. Nat. Neurosci. 10, 321–330 (2007).
  CAS PubMed PubMed Central Google Scholar
• Fields, R.D. & Ni, Y. Nonsynaptic communication through ATP release from volume-activated anion channels in axons. Sci. Signal. 3, ra73 (2010).
  PubMed PubMed Central Google Scholar
• Stevens, B. & Fields, R.D. Response of Schwann cells to action potentials in development. Science 287, 2267–2271 (2000).
  CAS PubMed Google Scholar
• Stevens, B., Porta, S., Haak, L.L., Gallo, V. & Fields, R.D. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36, 855–868 (2002).
  CAS PubMed PubMed Central Google Scholar
• Ishibashi, T. et al. Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823–832 (2006).
  CAS PubMed PubMed Central Google Scholar
• Taveggia, C., Feltri, M.L. & Wrabetz, L. Signals to promote myelin formation and repair. Nat. Rev. Neurol. 6, 276–287 (2010).
  PubMed PubMed Central Google Scholar
• Nave, K.A. Myelination and support of axonal integrity by glia. Nature 468, 244–252 (2010).
  CAS PubMed Google Scholar
• Emery, B. Regulation of oligodendrocyte differentiation and myelination. Science 330, 779–782 (2010).
  CAS PubMed Google Scholar
• Back, S.A., Luo, N.L., Borenstein, N.S., Volpe, J.J. & Kinney, H.C. Arrested oligodendrocyte lineage progression during human cerebral white matter development: dissociation between the timing of progenitor differentiation and myelinogenesis. J. Neuropathol. Exp. Neurol. 61, 197–211 (2002).
  PubMed Google Scholar
• Itoh, K., Stevens, B., Schachner, M. & Fields, R.D. Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 270, 1369–1372 (1995).
  CAS PubMed Google Scholar
• Wake, H., Lee, P.R. & Fields, R.D. Control of local protein synthesis and initial events in myelination by action potentials. Science 333, 1647–1651 (2011).
  CAS PubMed PubMed Central Google Scholar
• Dutta, R. & Trapp, B.D. Pathogenesis of axonal and neuronal damage in multiple sclerosis. Neurology 68, S22–S31; discussion S43–S54 (2007).
  PubMed Google Scholar
• Petrinovic, M.M. et al. Neuronal Nogo-A regulates neurite fasciculation, branching and extension in the developing nervous system. Development 137, 2539–2550 (2010).
  CAS PubMed Google Scholar
• Lee, H. et al. Synaptic function for the Nogo-66 receptor NgR1: regulation of dendritic spine morphology and activity-dependent synaptic strength. J. Neurosci. 28, 2753–2765 (2008).
  CAS PubMed PubMed Central Google Scholar
• Kang, X., Herron, T.J. & Woods, D.L. Regional variation, hemispheric asymmetries and gender differences in pericortical white matter. Neuroimage 56, 2011–2023 (2011).
  PubMed Google Scholar
• Laule, C. et al. Magnetic resonance imaging of myelin. Neurotherapeutics 4, 460–484 (2007).
  CAS PubMed PubMed Central Google Scholar
• Stankoff, B. et al. Imaging central nervous system myelin by positron emission tomography in multiple sclerosis using [methyl-11C]-2-(4′-methylaminophenyl)-6-hydroxybenzothiazole. Ann. Neurol. 69, 673–680 (2011).
  CAS PubMed Google Scholar
• Duyn, J.H. et al. High-field MRI of brain cortical substructure based on signal phase. Proc. Natl. Acad. Sci. USA 104, 11796–11801 (2007).
  CAS PubMed PubMed Central Google Scholar
• Van Leemput, K. et al. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 19, 549–557 (2009).
  PubMed PubMed Central Google Scholar
• Barazany, D., Basser, P.J. & Assaf, Y. In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 132, 1210–1220 (2009).
  PubMed PubMed Central Google Scholar
• Avram, A.V., Guidon, A. & Song, A.W. Myelin water weighted diffusion tensor imaging. Neuroimage 53, 132–138 (2010).
  PubMed Google Scholar
• Johansen-Berg, H., Della-Maggiore, V., Behrens, T.E., Smith, S.M. & Paus, T. Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage 36 (suppl. 2), T16–T21 (2007).
  PubMed Google Scholar
• Flöel, A., de Vries, M.H., Scholz, J., Breitenstein, C. & Johansen-Berg, H. White matter integrity in the vicinity of Broca's area predicts grammar learning success. Neuroimage 47, 1974–1981 (2009).
  PubMed Google Scholar
• Boyke, J., Driemeyer, J., Gaser, C., Buchel, C. & May, A. Training-induced brain structure changes in the elderly. J. Neurosci. 28, 7031–7035 (2008).
  CAS PubMed PubMed Central Google Scholar
• Wright, I.C. et al. A voxel-based method for the statistical analysis of gray and white matter density applied to schizophrenia. Neuroimage 2, 244–252 (1995).
  CAS PubMed Google Scholar
• Johansen-Berg, H. & Behrens, T.E.J. Diffusion MRI: From Quantitative Measurement to In Vivo Neuroanatomy (Elsevier, London, 2009).
• Horsfield, M.A. Magnetization transfer imaging in multiple sclerosis. J. Neuroimaging 15, 58S–67S (2005).
  PubMed Google Scholar
• Ashburner, J. et al. Identifying global anatomical differences: deformation-based morphometry. Hum. Brain Mapp. 6, 348–357 (1998).
  CAS PubMed PubMed Central Google Scholar
• Lohmann, G., von Cramon, D.Y. & Steinmetz, H. Sulcal variability of twins. Cereb. Cortex 9, 754–763 (1999).
  CAS PubMed Google Scholar
• Thomas, A.G. et al. Functional but not structural changes associated with learning: an exploration of longitudinal voxel-based morphometry (VBM). Neuroimage 48, 117–125 (2009).
  PubMed Google Scholar
• Johansen-Berg, H. Behavioural relevance of variation in white matter microstructure. Curr. Opin. Neurol. 23, 351–358 (2010).
  PubMed Google Scholar
• Maguire, E.A. et al. Navigation expertise and the human hippocampus: a structural brain imaging analysis. Hippocampus 13, 250–259 (2003).
  PubMed Google Scholar
• Bohbot, V.D., Lerch, J., Thorndycraft, B., Iaria, G. & Zijdenbos, A.P. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J. Neurosci. 27, 10078–10083 (2007).
  CAS PubMed PubMed Central Google Scholar
• Hyde, K.L. et al. Musical training shapes structural brain development. J. Neurosci. 29, 3019–3025 (2009).
  CAS PubMed PubMed Central Google Scholar