Longitudinal brain structure and cognitive changes over 8 years in an East Asian cohort

ABSTRACT Although East Asia harbors the largest number of aging adults in the world, there is currently little data clarifying the longitudinal brain‐cognition relationships in this group. Here, we report structural MRI and neuropsychological findings from relatively healthy Chinese older adults of the Singapore‐Longitudinal Aging Brain Study cohort over 8 years of follow up (n=111, mean age=67.1 years, range=56.1–83.1 years at baseline). Aging‐related change in structural volume was observed, with total cerebral atrophy at −0.56%/year, hippocampal atrophy at −0.94%/year and ventricular expansion at 3.56%/year. Only speed of processing showed an aging‐related decline, while other cognitive domains were relatively maintained. Faster decline in global cognition was associated with total cerebral, hippocampal and gray matter volume losses over time. Faster total cerebral atrophy and white matter atrophy (frontal and parietal regions) was associated with faster decline in verbal memory. Hippocampal atrophy and ventricular expansion were both associated with greater decline in verbal memory and executive function. Our findings provide a benchmark for research on brain structural and cognitive changes with aging in East Asians. HIGHLIGHTSCommunity‐based East Asian cohort with 8 years of brain MRI and cognitive test data.Decline in processing speed but not executive function, attention and memory.Rates of brain atrophy comparable to studies on Caucasians.Faster cerebral and white matter atrophy were related to faster decline in verbal memory.Hippocampal and ventricular changes were related to verbal memory and executive function decline.

[1]  E. Gordon,et al.  Regional White Matter and Neuropsychological Functioning across the Adult Lifespan , 2006, Biological Psychiatry.

[2]  Michael W. L. Chee,et al.  Cognitive function and brain structure correlations in healthy elderly East Asians , 2009, NeuroImage.

[3]  F. Lalonde,et al.  Effect of apolipoprotein E genotype on hippocampal volume loss in aging healthy women , 2001, Neurology.

[4]  B Winblad,et al.  Apolipoprotein E-epsilon 4 gene dose. , 1995, Lancet.

[5]  C. Jack,et al.  Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease , 1998, Neurology.

[6]  David A. Bennett,et al.  Association of white matter hyperintensities and gray matter volume with cognition in older individuals without cognitive impairment , 2015, Brain Structure and Function.

[7]  Yvonne Brehmer,et al.  Plasticity of brain and cognition in older adults , 2014, Psychological Research.

[8]  S. Resnick,et al.  Differential trajectories of age-related changes in components of executive and memory processes. , 2012, Psychology and aging.

[9]  N. Raz,et al.  Differential Aging of the Brain: Patterns, Cognitive Correlates and Modifiers , 2022 .

[10]  Mark A Espeland,et al.  Concurrent and longitudinal relationships between cognitive activity, cognitive performance, and brain volume in older adult women. , 2014, The journals of gerontology. Series B, Psychological sciences and social sciences.

[11]  R. Morris,et al.  Diffusion tensor imaging detects age related white matter change over a 2 year follow-up which is associated with working memory decline , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[12]  A. Smith.  Symbol Digit Modalities Test , 2016 .

[13]  E. Plante,et al.  Memory and executive function in older adults: relationships with temporal and prefrontal gray matter volumes and white matter hyperintensities , 2004, Neuropsychologia.

[14]  Hui Zheng,et al.  Differential age-dependent associations of gray matter volume and white matter integrity with processing speed in healthy older adults , 2015, NeuroImage.

[15]  John T. O'Brien,et al.  Progressive cortical thinning and subcortical atrophy in dementia with Lewy bodies and Alzheimer's disease , 2015, Neurobiology of Aging.

[16]  Shantanu H. Joshi,et al.  Mapping ventricular expansion onto cortical gray matter in older adults , 2015, Neurobiology of Aging.

[17]  Donald T. Stuss,et al.  Executive functions and the frontal lobes: a conceptual view , 2000, Psychological research.

[18]  Faiza Admiraal-Behloul,et al.  Ventricular dilation: Association with gait and cognition , 2009, Annals of neurology.

[19]  Amity E. Green,et al.  Hippocampal Atrophy and Ventricular Enlargement in Normal Aging, Mild Cognitive Impairment (MCI), and Alzheimer Disease , 2012, Alzheimer disease and associated disorders.

[20]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[21]  M. Lezak,et al.  Neuropsychological assessment, 4th ed. , 2004 .

[22]  I. Deary,et al.  What provides cerebral reserve? , 2004, Brain : a journal of neurology.

[23]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[24]  A. Dale,et al.  Effects of age on volumes of cortex, white matter and subcortical structures , 2005, Neurobiology of Aging.

[25]  Andreas Otte,et al.  The plasticity of the brain , 2001, European Journal of Nuclear Medicine.

[26]  David A. Bennett,et al.  Gray-matter macrostructure in cognitively healthy older persons: associations with age and cognition , 2013, Brain Structure and Function.

[27]  Owen Carmichael,et al.  TRAJECTORIES OF BRAIN LOSS IN AGING AND THE DEVELOPMENT OF COGNITIVE IMPAIRMENT , 2009, Neurology.

[28]  E. Kaplan,et al.  Delis-Kaplan Executive Function System , 2012 .

[29]  A. Dale,et al.  One-Year Brain Atrophy Evident in Healthy Aging , 2009, The Journal of Neuroscience.

[30]  Andrew R. Bender,et al.  White matter and memory in healthy adults: Coupled changes over two years , 2016, NeuroImage.

[31]  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.

[32]  J. Yesavage,et al.  Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. , 1986 .

[33]  T. Salthouse.  Selective review of cognitive aging , 2010, Journal of the International Neuropsychological Society.

[34]  S. Resnick,et al.  Longitudinal Magnetic Resonance Imaging Studies of Older Adults: A Shrinking Brain , 2003, The Journal of Neuroscience.

[35]  M. Weiner,et al.  Longitudinal Rates of Lobar Atrophy in Frontotemporal Dementia, Semantic Dementia, and Alzheimer's Disease , 2010, Alzheimer disease and associated disorders.

[36]  Annalisa Setti,et al.  Environment as ‘Brain Training’: A review of geographical and physical environmental influences on cognitive ageing , 2015, Ageing Research Reviews.

[37]  Alan C. Evans,et al.  A voxel-based morphometric study to determine individual differences in gray matter density associated with age and cognitive change over time. , 2004, Cerebral cortex.

[38]  Michael W. L. Chee,et al.  Hippocampal region-specific contributions to memory performance in normal elderly , 2010, Brain and Cognition.

[39]  P. Matthews,et al.  White matter lesion progression, brain atrophy, and cognitive decline: The Austrian stroke prevention study , 2005, Annals of neurology.

[40]  Kaarin J Anstey,et al.  COSMIC (Cohort Studies of Memory in an International Consortium): An international consortium to identify risk and protective factors and biomarkers of cognitive ageing and dementia in diverse ethnic and sociocultural groups , 2013, Alzheimer's & Dementia.

[41]  C. Studholme,et al.  Brain atrophy associated with baseline and longitudinal measures of cognition , 2011, Neurobiology of Aging.

[42]  D. Wedding.  Halstead‐Reitan Neuropsychological Test Battery , 2010 .

[43]  Ulman Lindenberger,et al.  Trajectories of brain aging in middle-aged and older adults: Regional and individual differences , 2010, NeuroImage.

[44]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[45]  M. Sliwinski,et al.  Understanding Ageing , 2001, Gerontology.

[46]  T. Salthouse,et al.  Executive functioning as a potential mediator of age-related cognitive decline in normal adults. , 2003, Journal of experimental psychology. General.

[47]  Paul M. Thompson,et al.  The apolipoprotein E epsilon 4 allele is associated with ventricular expansion rate and surface morphology in dementia and normal aging , 2014, Neurobiology of Aging.

[48]  Nicolas Cherbuin,et al.  A systematic review and meta-analysis of longitudinal hippocampal atrophy in healthy human ageing , 2015, NeuroImage.

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

[50]  S. Resnick,et al.  Longitudinal pattern of regional brain volume change differentiates normal aging from MCI , 2009, Neurology.

[51]  W. Sturm,et al.  Neuropsychological assessment , 2007, Journal of Neurology.

[52]  Carol Brayne,et al.  Operational definitions of successful aging: a systematic review , 2013, International Psychogeriatrics.

[53]  J. Barth,et al.  The Halstead-Reitan Neuropsychological Test Battery. , 2000 .

[54]  U. Lindenberger,et al.  Neuroanatomical correlates of fluid intelligence in healthy adults and persons with vascular risk factors. , 2008, Cerebral cortex.

[55]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[56]  Michael W Weiner,et al.  Longitudinal MRI and cognitive change in healthy elderly. , 2007, Neuropsychology.

[57]  Martin J Shipley,et al.  Change in sleep duration and cognitive function: findings from the Whitehall II Study. , 2011, Sleep.

[58]  D. Head,et al.  Differential aging of the medial temporal lobe , 2004, Neurology.

[59]  B. Roos,et al.  A Review of Selected Longitudinal Studies on Aging: Past Findings and Future Directions , 2010, Journal of the American Geriatrics Society.

[60]  Michael W. L. Chee,et al.  Reduced functional segregation between the default mode network and the executive control network in healthy older adults: A longitudinal study , 2016, NeuroImage.

[61]  C. Jack,et al.  Brain atrophy rates predict subsequent clinical conversion in normal elderly and amnestic MCI , 2005, Neurology.

[62]  C. Fennema-Notestine,et al.  Effects of age on tissues and regions of the cerebrum and cerebellum , 2001, Neurobiology of Aging.

[63]  A. Dale,et al.  Critical ages in the life course of the adult brain: nonlinear subcortical aging , 2013, Neurobiology of Aging.

[64]  N. Schuff,et al.  Longitudinal volumetric MRI change and rate of cognitive decline , 2005, Neurology.

[65]  Anders M. Fjell,et al.  Hippocampal volumes are important predictors for memory function in elderly women , 2009, BMC Medical Imaging.

[66]  Michael W Weiner,et al.  Memory in the aging brain: Doubly dissociating the contribution of the hippocampus and entorhinal cortex , 2007, Hippocampus.

[67]  Hugh S Markus,et al.  Verbal working and long-term episodic memory associations with white matter microstructure in normal aging investigated using tract-based spatial statistics. , 2013, Psychology and aging.

[68]  S. MacDonald,et al.  Intraindividual variability in cognitive performance in older adults: comparison of adults with mild dementia, adults with arthritis, and healthy adults. , 2000, Neuropsychology.

[69]  P. Matthews,et al.  Risk factors for progression of brain atrophy in aging , 2005, Neurology.

[70]  Albert Hofman,et al.  Cognitive Correlates of Ventricular Enlargement and Cerebral White Matter Lesions on Magnetic Resonance Imaging: The Rotterdam Study , 1994, Stroke.

[71]  Nick C Fox,et al.  Hippocampal atrophy rates in Alzheimer disease , 2009, Neurology.

[72]  Michael W. L. Chee,et al.  Brain Structure in Young and Old East Asians and Westerners: Comparisons of Structural Volume and Cortical Thickness , 2011, Journal of Cognitive Neuroscience.

[73]  C. Jack,et al.  Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. , 1989, Radiology.

[74]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[75]  Stephen M. Smith,et al.  Age-related changes in grey and white matter structure throughout adulthood , 2010, NeuroImage.

[76]  D. Delis,et al.  Posterior cingulum white matter disruption and its associations with verbal memory and stroke risk in mild cognitive impairment. , 2012, Journal of Alzheimer's disease : JAD.

[77]  N. Raz,et al.  Aging white matter and cognition: Differential effects of regional variations in diffusion properties on memory, executive functions, and speed , 2009, Neuropsychologia.

[78]  R. Reitan,et al.  3/The Halstead-Reitan Neuropsychological Test Battery and Aging , 1986 .

[79]  Hans-Jochen Heinze,et al.  Comparing manual and automatic segmentation of hippocampal volumes: Reliability and validity issues in younger and older brains , 2014, Human brain mapping.

[80]  Sam K. Y. Sim,et al.  Sleep duration and age-related changes in brain structure and cognitive performance. , 2014, Sleep.

[81]  C. Jack,et al.  Memory and MRI-based hippocampal volumes in aging and AD , 2000, Neurology.

[82]  T. Salthouse.  Neuroanatomical substrates of age-related cognitive decline. , 2011, Psychological bulletin.

[83]  John R. Crawford,et al.  The Executive Decline Hypothesis of Cognitive Aging: Do Executive Deficits Qualify as Differential Deficits and Do They Mediate Age-Related Memory Decline? , 2000 .

[84]  J. Schneider,et al.  Individual differences in rates of change in cognitive abilities of older persons. , 2002, Psychology and aging.