Age-related white-matter correlates of motor sequence learning and consolidation

Older adults show impaired consolidation in motor sequence learning (MSL) tasks, failing to demonstrate the sleep-dependent performance gains usually seen in young individuals. To date, few studies have investigated the white-matter substrates of MSL in healthy aging, and none have addressed how fiber pathways differences may contribute to the age-related consolidation deficit. Accordingly, we used diffusion-weighted magnetic resonance imaging to explore how white-matter characteristics relate to performance using an explicit MSL task in young and older participants. Analysis revealed that initial learning scores were correlated to white-matter microstructure in the corticospinal tract and within the corpus callosum regardless of age. Furthermore, sleep-dependent consolidation scores, in young adults only, were related to white-matter tract organization in a frontal area where several major fiber bundles cross each other. These findings further our understanding of the neural correlates of MSL in healthy aging and provide the first evidence that age-related white-matter differences in tract configuration may underlie the age-related motor memory consolidation deficit.

[1]  Richard B. Ivry,et al.  Sleep modulates word-pair learning but not motor sequence learning in healthy older adults , 2012, Neurobiology of Aging.

[2]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[3]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[4]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[5]  Richard B Ivry,et al.  Age-related decline of sleep-dependent consolidation. , 2007, Learning & memory.

[6]  R. E. Schmidt,et al.  Toward accurate diagnosis of white matter pathology using diffusion tensor imaging , 2007, Magnetic resonance in medicine.

[7]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[9]  G. Albouy,et al.  Daytime Sleep Enhances Consolidation of the Spatial but Not Motoric Representation of Motor Sequence Memory , 2013, PloS one.

[10]  Derek K. Jones,et al.  Estimating the number of fiber orientations in diffusion MRI voxels : a constrained spherical deconvolution study , 2010 .

[11]  Wang Zhan,et al.  Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis , 2010, Neurobiology of Aging.

[12]  P Maquet,et al.  The Role of Sleep in Learning and Memory , 2001, Science.

[13]  Jennifer R. Ramautar,et al.  Individual Differences in White Matter Diffusion Affect Sleep Oscillations , 2013, The Journal of Neuroscience.

[14]  Genevieve Albouy,et al.  fMRI and sleep correlates of the age‐related impairment in motor memory consolidation , 2014, Human brain mapping.

[15]  R. Stickgold,et al.  Sleep-Dependent Learning and Memory Consolidation , 2004, Neuron.

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

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

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

[19]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

[20]  Chandan J. Vaidya,et al.  White matter integrity correlates of implicit sequence learning in healthy aging , 2011, Neurobiology of Aging.

[21]  Heidi Johansen-Berg,et al.  Structural and functional bases for individual differences in motor learning , 2011, Human brain mapping.

[22]  Daniel Z. Press,et al.  Sequence Skill Acquisition and Off-Line Learning in Normal Aging , 2009, PloS one.

[23]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[24]  G. Albouy,et al.  Neural correlates of the age-related changes in motor sequence learning and motor adaptation in older adults , 2013, Front. Hum. Neurosci..

[25]  K Rickels,et al.  Short form of depression inventory: cross-validation. , 1974, Psychological reports.

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

[27]  Klaus H. Maier-Hein,et al.  Methodological considerations on tract-based spatial statistics (TBSS) , 2014, NeuroImage.

[28]  M. Folstein,et al.  Mini-Mental State Examination (MMSE) , 2019, Encyclopedia of Gerontology and Population Aging.

[29]  Heidi Johansen-Berg,et al.  The rate of visuomotor adaptation correlates with cerebellar white‐matter microstructure , 2009, Human brain mapping.

[30]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

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

[32]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[33]  Sunbin Song,et al.  White matter microstructural correlates of superior long-term skill gained implicitly under randomized practice. , 2012, Cerebral cortex.

[34]  J. Rinne,et al.  Functional imaging studies of dopamine system and cognition in normal aging and Parkinson's disease , 2002, Neuroscience & Biobehavioral Reviews.

[35]  A. Maclean,et al.  Psychometric evaluation of the Stanford Sleepiness Scale , 1992, Journal of sleep research.

[36]  David F. Dinges,et al.  Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations , 1985 .

[37]  V. Penhune,et al.  Author's Personal Copy Behavioural Brain Research Parallel Contributions of Cerebellar, Striatal and M1 Mechanisms to Motor Sequence Learning , 2022 .

[38]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[39]  Habib Benali,et al.  Off-line consolidation of motor sequence learning results in greater integration within a cortico-striatal functional network , 2014, NeuroImage.

[40]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

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

[42]  Julien Doyon,et al.  Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems , 2015, NeuroImage.

[43]  Christian Gerloff,et al.  White matter integrity of motor connections related to training gains in healthy aging , 2014, Neurobiology of Aging.

[44]  Heidi Johansen-Berg,et al.  Structural correlates of skilled performance on a motor sequence task , 2012, Front. Hum. Neurosci..

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

[46]  Matthew P Walker,et al.  A refined model of sleep and the time course of memory formation. , 2005, The Behavioral and brain sciences.

[47]  Karolina Janacsek,et al.  The dynamics of implicit skill consolidation in young and elderly adults. , 2011, The journals of gerontology. Series B, Psychological sciences and social sciences.

[48]  Maxime Descoteaux,et al.  Dipy, a library for the analysis of diffusion MRI data , 2014, Front. Neuroinform..

[49]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[50]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[51]  A. Karni The acquisition of perceptual and motor skills: a memory system in the adult human cortex. , 1996, Brain research. Cognitive brain research.

[52]  Leslie G. Ungerleider,et al.  Brain plasticity related to the consolidation of motor sequence learning and motor adaptation , 2010, Proceedings of the National Academy of Sciences.

[53]  Leslie G. Ungerleider,et al.  Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning , 2009, Experimental Brain Research.

[54]  Ovidiu Lungu,et al.  Changes in spinal reflex excitability associated with motor sequence learning. , 2010, Journal of neurophysiology.

[55]  Ruiwang Huang,et al.  Long-term intensive training induced brain structural changes in world class gymnasts , 2015, Brain Structure and Function.

[56]  Lars Bäckman,et al.  Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: Relations to performance , 2010, NeuroImage.

[57]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[58]  Stephen M. Smith,et al.  Crossing fibres in tract-based spatial statistics , 2010, NeuroImage.

[59]  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.

[60]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[61]  Hauke R. Heekeren,et al.  Age-related differences in white matter microstructure: Region-specific patterns of diffusivity , 2010, NeuroImage.

[62]  Leslie G. Ungerleider,et al.  Imaging Brain Plasticity during Motor Skill Learning , 2002, Neurobiology of Learning and Memory.

[63]  M. Desseilles,et al.  Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory , 2008, Neuron.

[64]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[65]  H. Johansen-Berg,et al.  Accelerated Changes in White Matter Microstructure during Aging: A Longitudinal Diffusion Tensor Imaging Study , 2014, The Journal of Neuroscience.

[66]  D. Howard,et al.  Age differences in learning serial patterns: direct versus indirect measures. , 1989, Psychology and Aging.

[67]  Julien Cohen-Adad,et al.  Simultaneous Brain–Cervical Cord fMRI Reveals Intrinsic Spinal Cord Plasticity during Motor Sequence Learning , 2015, PLoS biology.

[68]  Christian Keysers,et al.  Inter‐individual differences in audio‐motor learning of piano melodies and white matter fiber tract architecture , 2014, Human brain mapping.

[69]  Á. Pascual-Leone,et al.  Awareness Modifies the Skill-Learning Benefits of Sleep , 2004, Current Biology.

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

[71]  Faith M. Gunning-Dixon,et al.  Differential aging of the human striatum: a prospective MR imaging study. , 1998, AJNR. American journal of neuroradiology.

[72]  J. Ashe,et al.  Cerebellum Activation Associated with Performance Change but Not Motor Learning , 2002, Science.

[73]  Lars Bäckman,et al.  Implicit Learning in Aging: Extant Patterns and New Directions , 2009, Neuropsychology Review.

[74]  V. Penhune,et al.  Specific Increases within Global Decreases: A Functional Magnetic Resonance Imaging Investigation of Five Days of Motor Sequence Learning , 2010, The Journal of Neuroscience.

[75]  A. Beck,et al.  An inventory for measuring clinical anxiety: psychometric properties. , 1988, Journal of consulting and clinical psychology.