Rapid language-related plasticity: microstructural changes in the cortex after a short session of new word learning

Human brain imaging revealed that the brain can undergo structural plasticity following new learning experiences. Most magnetic resonance imaging (MRI) uncovered morphometric alternation in cortical density after the long-term training of weeks to months. A recent diffusion tensor imaging (DTI) study has found changes in diffusion indices after 2 h of training, primarily in the hippocampus. However, whether a short learning experience can induce microstructural changes in the neocortex is still unclear. Here, we used diffusion MRI, a method sensitive to tissue microstructure, to study cortical plasticity. To attain cortical involvement, we used a short language task (under 1 h) of introducing new lexical items (flower names) to the lexicon. We have found significant changes in diffusivity in cortical regions involved in language and reading (inferior frontal gyrus, middle temporal gyrus, and inferior parietal lobule). In addition, the difference in the values of diffusivity correlated with the lexical learning rate in the task. Moreover, significant changes were found in white matter tracts near the cortex, and the extent of change correlated with behavioral measures of lexical learning rate. These findings provide first evidence of short-term cortical plasticity in the human brain after a short language learning task. It seems that short training of less than an hour of high cognitive demand can induce microstructural changes in the cortex, suggesting a rapid time scale of neuroplasticity and providing additional evidence of the power of MRI to investigate the temporal and spatial progressions of this process.

[1]  W. Levelt Accessing words in speech production: Stages, processes and representations , 1992, Cognition.

[2]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[3]  Richard S. J. Frackowiak,et al.  Neurolinguistics: Structural plasticity in the bilingual brain , 2004, Nature.

[4]  Edward H Herskovits,et al.  Neural regions essential for reading and spelling of words and pseudowords , 2007, Annals of neurology.

[5]  Willem J. M. Levelt,et al.  The neural correlates of language production , 2000 .

[6]  H. Gardner,et al.  Language and Learning: The Debate between Jean Piaget and Noam Chomsky , 1983 .

[7]  Peter U. Tse,et al.  White Matter Structure Changes as Adults Learn a Second Language , 2012, Journal of Cognitive Neuroscience.

[8]  Thomas Roeper,et al.  Theoretical Issues in Language Acquisition : Continuity and Change in Development , 1992 .

[9]  Brian Butterworth,et al.  Disorders of phonological encoding , 1992, Cognition.

[10]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[11]  David Poeppel,et al.  Towards a new functional anatomy of language , 2004, Cognition.

[12]  Noam Chomsky Knowledge of language: its nature, origin, and use , 1988 .

[13]  Thomas Wolbers,et al.  Hippocampus activity differentiates good from poor learners of a novel lexicon , 2005, NeuroImage.

[14]  Grant M. Walker,et al.  Anterior temporal involvement in semantic word retrieval: voxel-based lesion-symptom mapping evidence from aphasia. , 2009, Brain : a journal of neurology.

[15]  Peter Indefrey,et al.  The Spatial and Temporal Signatures of Word Production Components: A Critical Update , 2011, Front. Psychology.

[16]  Steve Majerus,et al.  Modulation of brain activity during phonological familiarization , 2005, Brain and Language.

[17]  Riitta Salmelin,et al.  Accessing newly learned names and meanings in the native language , 2009, Human brain mapping.

[18]  Gregory Hickok,et al.  Neural correlates of word production stages delineated by parametric modulation of psycholinguistic variables , 2009, Human brain mapping.

[19]  H. Buckingham The Marc Dax (1770–1837)/Paul Broca (1824–1880) controversy over priority in science: Left hemisphere specificity for seat of articulate language and for lesions that cause aphemia , 2006, Clinical linguistics & phonetics.

[20]  I. Tasaki,et al.  Volume expansion of nonmyelinated nerve fibers during impulse conduction. , 1990, Biophysical journal.

[21]  G. Knott,et al.  Plasticity of Astrocytic Coverage and Glutamate Transporter Expression in Adult Mouse Cortex , 2006, PLoS biology.

[22]  S. Freytag Knowledge Of Language Its Nature Origin And Use , 2016 .

[23]  A. Rodríguez-Fornells,et al.  Watching the brain during meaning acquisition. , 2007, Cerebral cortex.

[24]  Lyndsey Nickels,et al.  A frequent occurrence? factors affecting the production of semantic errors in aphasic naming , 1994 .

[25]  Eduardo D. Martín,et al.  Structural and Functional Plasticity of Astrocyte Processes and Dendritic Spine Interactions , 2014, The Journal of Neuroscience.

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

[27]  Riitta Salmelin,et al.  Learning new names for new objects: Cortical effects as measured by magnetoencephalography , 2004, Brain and Language.

[28]  Magnus Lindgren,et al.  Growth of language-related brain areas after foreign language learning , 2012, NeuroImage.

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

[30]  Matti Laine,et al.  Naming of newly learned objects: a PET activation study. , 2005, Brain research. Cognitive brain research.

[31]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[32]  Sven Joubert,et al.  Neural correlates of lexical and sublexical processes in reading , 2004, Brain and Language.

[33]  Grzegorz Dogil,et al.  Functional imaging of language competentbrain areas , 2009 .

[34]  S. Ge,et al.  Neurogenesis and hippocampal plasticity in adult brain. , 2013, Current topics in behavioral neurosciences.

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

[36]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[37]  S. Oliet,et al.  Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. , 2008, Physiological reviews.

[38]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

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

[41]  Richard S. J. Frackowiak,et al.  Brain activity during reading. The effects of exposure duration and task. , 1994, Brain : a journal of neurology.

[42]  Noam Chomsky Three Factors in Language Design , 2005, Linguistic Inquiry.

[43]  Antoni Rodríguez-Fornells,et al.  Word learning is mediated by the left arcuate fasciculus , 2013, 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]  A. Ardila,et al.  The role of the arcuate fasciculus in conduction aphasia. , 2009, Brain : a journal of neurology.

[46]  C. Price The functional anatomy of word comprehension and production , 1998, Trends in Cognitive Sciences.

[47]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

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

[49]  Heidi Johansen-Berg,et al.  Fornix Microstructure Correlates with Recollection But Not Familiarity Memory , 2009, The Journal of Neuroscience.

[50]  Ethan R. Buch,et al.  Cortical and subcortical interactions during action reprogramming and their related white matter pathways , 2010, Proceedings of the National Academy of Sciences.

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

[52]  C. Büchel,et al.  Temporal and Spatial Dynamics of Brain Structure Changes during Extensive Learning , 2006, The Journal of Neuroscience.

[53]  Lyndsey Nickels,et al.  Spoken Word Production and Its Breakdown In Aphasia , 1997 .

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

[55]  David G. Norris,et al.  Functional connectivity between brain regions involved in learning words of a new language , 2010, Brain and Language.

[56]  A. Damasioa,et al.  Neural systems behind word and concept retrieval , 2004 .

[57]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

[58]  Matthew H. Davis,et al.  Learning and Consolidation of Novel Spoken Words , 2009, Journal of Cognitive Neuroscience.

[59]  N. Friedmann,et al.  The Cambridge Handbook of Biolinguistics: Lexical retrieval and its breakdown in aphasia and developmental language impairment , 2013 .

[60]  U. Bellugi,et al.  The linguistic basis of left hemisphere specialization. , 1992, Science.

[61]  A. Friederici The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[62]  R. Fields,et al.  Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. , 2002, Neuron.

[63]  S. Crain Language acquisition in the absence of experience , 1991, Behavioral and Brain Sciences.

[64]  Karl J. Friston,et al.  The cortical localization of the lexicons. Positron emission tomography evidence. , 1992, Brain : a journal of neurology.

[65]  Cristina Burani,et al.  Supercalifragilisticexpialidocious: How the brain learns words never heard before , 2009, NeuroImage.

[66]  J. Millichap,et al.  Brain Activity During Reading , 1995 .

[67]  Derek K. Jones,et al.  Interindividual Variation in Fornix Microstructure and Macrostructure Is Related to Visual Discrimination Accuracy for Scenes But Not Faces , 2014, The Journal of Neuroscience.

[68]  Maria Stein,et al.  Structural plasticity in the language system related to increased second language proficiency , 2012, Cortex.

[69]  G. Altmann,et al.  The Oxford Handbook of Psycholinguistics , 2007 .

[70]  M. Garrett,et al.  Lexical retrieval and its breakdown in aphasia and developmental language impairment , 2013 .

[71]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[72]  Marlene Behrmann,et al.  Localization in alexia. , 1994 .

[73]  R. Douglas Fields,et al.  Control of Local Protein Synthesis and Initial Events in Myelination by Action Potentials , 2011, Science.

[74]  A. Hillis,et al.  Neural regions essential for distinct cognitive processes underlying picture naming. , 2007, Brain : a journal of neurology.

[75]  Friedemann Pulvermüller,et al.  Rapid Cortical Plasticity Underlying Novel Word Learning , 2010, The Journal of Neuroscience.

[76]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[77]  Yury Shtyrov,et al.  Fast Mapping of Novel Word Forms Traced Neurophysiologically , 2011, Front. Psychology.

[78]  A. Mechelli,et al.  Anatomical Traces of Vocabulary Acquisition in the Adolescent Brain , 2007, The Journal of Neuroscience.

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

[80]  Mart Bles,et al.  Phonological processing of ignored distractor pictures, an fMRI investigation , 2008, BMC Neuroscience.

[81]  John Ashburner,et al.  Structural plasticity in the bilingual brain: Proficiency in a second language and age at acquisition affect grey-matter density. , 2004 .

[82]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[83]  A. May Experience-dependent structural plasticity in the adult human brain , 2011, Trends in Cognitive Sciences.

[84]  Peter Indefrey,et al.  Brain-imaging studies of language production , 2007 .