Age related differences in reaction time components and diffusion properties of normal-appearing white matter in healthy adults

Deterioration of the white matter (WM) is viewed as the neural substrate of age differences in speed of information processing (reaction time, RT). However, the relationship between WM and RT components is rarely examined in healthy aging. We assessed the relationship between RT components derived from the Ratcliff diffusion model and micro-structural properties of normal-appearing WM (NAWM) in 90 healthy adults (age 18-82 years). We replicated all major extant findings pertaining to age differences in RT components and WM: lower drift rate, greater response conservativeness, longer non-decision time, lower fractional anisotropy (FA), greater mean (MD), axial (AD) and radial (RD) diffusivity were associated with advanced age. Age differences in anterior regions of the cerebral WM exceeded those in posterior regions. However, the only relationship between RT components and WM was the positive association between DR in the body of the corpus callosum and non-decision time. Thus, in healthy adults, age differences in NAWM diffusion properties are not a major contributor to age differences in RT components. Longitudinal studies with more precise and specific estimates of regional myelin content and evaluation of the contribution of age-related vascular risk factors are necessary to understand cerebral substrates of age-related cognitive slowing.

[1]  F. Donders On the speed of mental processes. , 1969, Acta psychologica.

[2]  Naftali Raz,et al.  Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk , 2009, Brain Research.

[3]  B B Reiss,et al.  The reliability and validity of the Mini-Mental State in a British community survey. , 1989, Journal of psychiatric research.

[4]  R. Ratcliff,et al.  A diffusion model analysis of the effects of aging on letter discrimination. , 2003, Psychology and aging.

[5]  R. Ratcliff,et al.  Aging and individual differences in rapid two-choice decisions , 2006, Psychonomic bulletin & review.

[6]  Karen M Rodrigue,et al.  Vascular health and longitudinal changes in brain and cognition in middle-aged and older adults. , 2007, Neuropsychology.

[7]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[8]  D. Head,et al.  Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. , 2004, Cerebral cortex.

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

[10]  R. Ratcliff,et al.  The effects of aging on reaction time in a signal detection task. , 2001, Psychology and aging.

[11]  L. Radloff The CES-D Scale , 1977 .

[12]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[13]  Francis Tuerlinckx,et al.  Diffusion model analysis with MATLAB: A DMAT primer , 2008, Behavior research methods.

[14]  S. Maxwell,et al.  Bias in cross-sectional analyses of longitudinal mediation. , 2007, Psychological methods.

[15]  Brian Lawlor,et al.  Rating scales in old age psychiatry , 2002, British Journal of Psychiatry.

[16]  Thomas R. Knösche,et al.  White matter integrity, fiber count, and other fallacies: The do's and don'ts of diffusion MRI , 2013, NeuroImage.

[17]  Roberto Cabeza,et al.  Assessing the effects of age on long white matter tracts using diffusion tensor tractography , 2009, NeuroImage.

[18]  Blair Saunders,et al.  False external feedback modulates posterror slowing and the f-P300: implications for theories of posterror adjustment , 2012, Psychonomic bulletin & review.

[19]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[20]  F. Gunning-Dixon,et al.  The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. , 2000, Neuropsychology.

[21]  E. Wagenmakers,et al.  Psychological interpretation of the ex-Gaussian and shifted Wald parameters: A diffusion model analysis , 2009, Psychonomic bulletin & review.

[22]  S. Sternberg Memory-scanning: mental processes revealed by reaction-time experiments. , 1969, American scientist.

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

[24]  Derek K. Jones,et al.  Why diffusion tensor MRI does well only some of the time: Variance and covariance of white matter tissue microstructure attributes in the living human brain☆ , 2014, NeuroImage.

[25]  A. Pfefferbaum,et al.  Diffusion tensor imaging and aging , 2006, Neuroscience & Biobehavioral Reviews.

[26]  Roger Ratcliff,et al.  Application of the diffusion model to two-choice tasks for adults 75-90 years old. , 2007, Psychology and aging.

[27]  Wiro J. Niessen,et al.  White matter atrophy and lesion formation explain the loss of structural integrity of white matter in aging , 2008, NeuroImage.

[28]  Timothy A. Salthouse,et al.  Theoretical Perspectives on Cognitive Aging , 1991 .

[29]  Hellmut Merkle,et al.  Tracking iron in multiple sclerosis: a combined imaging and histopathological study at 7 Tesla. , 2011, Brain : a journal of neurology.

[30]  R. Ratcliff Modeling aging effects on two-choice tasks: response signal and response time data. , 2008, Psychology and aging.

[31]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[32]  Karen M Rodrigue,et al.  Hypertension and the brain: vulnerability of the prefrontal regions and executive functions. , 2003, Behavioral neuroscience.

[33]  A. Song,et al.  Cerebral White Matter Integrity and Cognitive Aging: Contributions from Diffusion Tensor Imaging , 2009, Neuropsychology Review.

[34]  Owen Carmichael,et al.  FLAIR and Diffusion MRI Signals Are Independent Predictors of White Matter Hyperintensities , 2013, American Journal of Neuroradiology.

[35]  Roger Ratcliff,et al.  The EZ diffusion method: Too EZ? , 2008, Psychonomic bulletin & review.

[36]  Richa Trivedi,et al.  Quantification of age- and gender-related changes in diffusion tensor imaging indices in deep grey matter of the normal human brain , 2011, Journal of Clinical Neuroscience.

[37]  A. Green,et al.  Effects of diffuse axonal injury on speed of information processing following severe traumatic brain injury. , 2004, Neuropsychology.

[38]  H Takao,et al.  Effects of Age and Gender on White Matter Integrity , 2011, American Journal of Neuroradiology.

[39]  Scott A. Huettel,et al.  Age-related slowing of memory retrieval: Contributions of perceptual speed and cerebral white matter integrity , 2008, Neurobiology of Aging.

[40]  A. Voss,et al.  Interpreting the parameters of the diffusion model: An empirical validation , 2004, Memory & cognition.

[41]  E. Wagenmakers,et al.  Testing theories of post-error slowing , 2011, Attention, perception & psychophysics.

[42]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[43]  J. Cerella Information processing rates in the elderly. , 1985, Psychological bulletin.

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

[45]  Roberto Cabeza,et al.  The architecture of cross-hemispheric communication in the aging brain: linking behavior to functional and structural connectivity. , 2012, Cerebral cortex.

[46]  Torsten Rohlfing,et al.  Longitudinal Study of Callosal Microstructure in the Normal Adult Aging Brain Using Quantitative DTI Fiber Tracking , 2010, Developmental neuropsychology.

[47]  C. Wheeler-Kingshott,et al.  About “axial” and “radial” diffusivities , 2009, Magnetic resonance in medicine.

[48]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[49]  P. Bentler,et al.  Cutoff criteria for fit indexes in covariance structure analysis : Conventional criteria versus new alternatives , 1999 .

[50]  T. Salthouse Converging evidence for information-processing stages: A comparative-influence stage-analysis method , 1981 .

[51]  R Ratcliff,et al.  The effects of aging on reaction time in a signal detection task. , 2001, Psychology and aging.

[52]  G. Kerchner,et al.  Cognitive Processing Speed in Older Adults: Relationship with White Matter Integrity , 2012, PloS one.

[53]  Roland Bammer,et al.  Cognitive processing speed and the structure of white matter pathways: Convergent evidence from normal variation and lesion studies , 2008, NeuroImage.

[54]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[55]  T. Salthouse,et al.  Adult age and the speed-accuracy trade-off. , 1979, Ergonomics.

[56]  Xavier Golay,et al.  Reduced R2′ in multiple sclerosis normal appearing white matter and lesions may reflect decreased myelin and iron content , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[57]  U. Lindenberger,et al.  Cross-sectional age variance extraction: what's change got to do with it? , 2011, Psychology and aging.

[58]  Roberto Cabeza,et al.  Cerebral White Matter Integrity Mediates Adult Age Differences in Cognitive Performance , 2009, Journal of Cognitive Neuroscience.

[59]  K. Warner Schaie,et al.  Perceptual speed in adulthood: cross-sectional and longitudinal studies. , 1989, Psychology and aging.

[60]  Paul M. Thompson,et al.  Genetics of white matter development: A DTI study of 705 twins and their siblings aged 12 to 29 , 2011, NeuroImage.

[61]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[62]  Ofer Pasternak,et al.  Structural correlates of memory performance with diffusion tensor imaging , 2009, NeuroImage.

[63]  Edith V. Sullivan,et al.  Equivalent disruption of regional white matter microstructure in ageing healthy men and women , 2001, Neuroreport.

[64]  Ricardo Tarrasch,et al.  Structural correlates of cognitive domains in normal aging with diffusion tensor imaging , 2011, Brain Structure and Function.