The rapid development of structural plasticity through short water maze training: A DTI study

ABSTRACT Diffusion MRI is sensitive to the microstructure of tissue and allows the study of structural plasticity over short time scales of only hours. The initial temporal and spatial progression of this process, however, has yet to be elucidated. With the aim of examining early temporal progression of structural plasticity, we subjected rats to short training periods on a task in the Morris water maze (MWM), a paradigm previously shown to induce rapid changes in diffusion tensor imaging (DTI) indices. Two groups of rats were each divided into subgroups that consecutively completed 1, 2 or 3 sets of short trials (up to 60 s) in the MWM. Each set comprised 4 trials (1 from each quadrant of the WMW), with a specific time interval between sets. To assess the effect of the duration of the task on the evolving changes in DTI indices, we allowed a rest of 45 min between sets in one group of rats and a 2‐h rest in the other. All rats were scanned with a DTI protocol before and 45 min after their last trial. We found that a few minutes of training in a new task sufficed to generate changes in diffusion indices. The earliest changes in DTI (measured after one set of trials) progressed with further training (measured after two sets), but within a few more minutes (after three sets) they reached a plateau. Lengthening the duration of the overall task by prolonging the time interval between sessions did not alter this pattern of change, suggesting that at least within this short time scale such changes are task‐dependent, but not time dependent. Our results demonstrate the progression of structural neuroplasticity at different stages of exposure to a novel experience, and show that DTI can be used to trace, in vivo, the localization of structural plasticity induced by training.

[1]  Derek K. Jones,et al.  RESTORE: Robust estimation of tensors by outlier rejection , 2005, Magnetic resonance in medicine.

[2]  Takaki Komiyama,et al.  Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning , 2015, Nature Neuroscience.

[3]  J B Poline,et al.  Transient decrease in water diffusion observed in human occipital cortex during visual stimulation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

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

[8]  P. Caroni,et al.  Structural plasticity upon learning: regulation and functions , 2012, Nature Reviews Neuroscience.

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

[10]  D. Le Bihan.  The ‘wet mind’: water and functional neuroimaging , 2007, Physics in medicine and biology.

[11]  Yaniv Assaf,et al.  Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain , 2005, NeuroImage.

[12]  Karel Svoboda,et al.  Rapid Functional Maturation of Nascent Dendritic Spines , 2009, Neuron.

[13]  Arno Villringer,et al.  Advanced MRI techniques to improve our understanding of experience-induced neuroplasticity , 2016, NeuroImage.

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

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

[16]  L. Merabet,et al.  The plastic human brain cortex. , 2005, Annual review of neuroscience.

[17]  L P Noldus,et al.  EthoVision: A versatile video tracking system for automation of behavioral experiments , 2001, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[18]  Yaniv Assaf,et al.  Micro-structural assessment of short term plasticity dynamics , 2013, NeuroImage.

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

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

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

[22]  Naama Friedmann,et al.  Rapid language-related plasticity: microstructural changes in the cortex after a short session of new word learning , 2017, Brain Structure and Function.

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

[24]  R. D'Hooge,et al.  Applications of the Morris water maze in the study of learning and memory , 2001, Brain Research Reviews.

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

[26]  Marcel Adam Just,et al.  Structural and functional neuroplasticity in human learning of spatial routes , 2016, NeuroImage.

[27]  P. Basser,et al.  New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter , 2004, Magnetic resonance in medicine.

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

[29]  Bogdan Draganski,et al.  Training-induced structural changes in the adult human brain , 2008, Behavioural Brain Research.

[30]  Yaniv Assaf,et al.  Can we use diffusion MRI as a bio-marker of neurodegenerative processes? , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

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