Gray Matter Volume and Cognitive Performance During Normal Aging. A Voxel-Based Morphometry Study

Normal aging is characterized by decline in cognitive functioning in conjunction with extensive gray matter (GM) atrophy. A first aim of this study was to determine GM volume differences related to aging by comparing two groups of participants, middle-aged group (MAG, mean age 41 years, N = 16) and older adults (OG, mean age 71 years, N = 14) who underwent an magnetic resonance images (MRI) voxel-based morphometry (VBM) evaluation. The VBM analyses included two optimized pipelines, for the cortex and for the cerebellum. Participants were also evaluated on a wide range of cognitive tests assessing both domain-general and language-specific processes, in order to examine how GM volume differences between OG and MAG relate to cognitive performance. Our results show smaller bilateral GM volume in the OG relative to the MAG, in several cerebral and right cerebellar regions involved in language and executive functions. Importantly, our results also revealed smaller GM volume in the right cerebellum in OG relative to MAG, supporting the idea of a complex cognitive role for this structure. This study provides a broad picture of cerebral, but also cerebellar and cognitive changes associated with normal aging.

[1]  Yana Suchy,et al.  Age-related changes of the functional architecture of the cortico-basal ganglia circuitry during motor task execution , 2011, NeuroImage.

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

[3]  A. Krainik,et al.  Functional MRI evidence for the decline of word retrieval and generation during normal aging , 2015, AGE.

[4]  A. Krainik,et al.  Aging Modulates the Hemispheric Specialization during Word Production , 2017, Front. Aging Neurosci..

[5]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[6]  Y. Joanette,et al.  [Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level]. , 1990, Acta neurologica Belgica.

[7]  L. Nyberg,et al.  Longitudinal association between hippocampus atrophy and episodic-memory decline , 2017, Neurobiology of Aging.

[8]  F. Craik,et al.  Executive function across the life span. , 2004, Acta psychologica.

[9]  F. Collette,et al.  Relationship between grey matter integrity and executive abilities in aging , 2016, Brain Research.

[10]  Lukas Scheef,et al.  Volume reduction of the entorhinal cortex in subjective memory impairment , 2006, Neurobiology of Aging.

[11]  G. Winocur,et al.  Clustering and switching as two components of verbal fluency: evidence from younger and older healthy adults. , 1997, Neuropsychology.

[12]  A. Meyer-Lindenberg,et al.  Normal age-related brain morphometric changes: nonuniformity across cortical thickness, surface area and gray matter volume? , 2012, Neurobiology of Aging.

[13]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[14]  Conor V. Dolan,et al.  Source (or Part of the following Source): Type Article Title Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis Author(s) Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis , 2022 .

[15]  R. Katzman.,et al.  Education and the prevalence of dementia and Alzheimer's disease , 1993, Neurology.

[16]  A. Dale,et al.  What is normal in normal aging? Effects of aging, amyloid and Alzheimer's disease on the cerebral cortex and the hippocampus , 2014, Progress in Neurobiology.

[17]  S. D'Amore,et al.  [Hospital anxiety and depression]. , 2011, Reumatismo.

[18]  Frederik Maes,et al.  Assessing age-related gray matter decline with voxel-based morphometry depends significantly on segmentation and normalization procedures , 2014, Front. Aging Neurosci..

[19]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[20]  G. Kavé,et al.  The association between age and the frequency of nouns selected for production. , 2009, Psychology and aging.

[21]  J. Morris,et al.  Recent publications from the Alzheimer's Disease Neuroimaging Initiative: Reviewing progress toward improved AD clinical trials , 2017, Alzheimer's & Dementia.

[22]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[23]  Gregory Hickok,et al.  The functional neuroanatomy of language. , 2009, Physics of life reviews.

[24]  J. Bryan,et al.  Measures of fluency as predictors of incidental memory among older adults. , 2000, Psychology and aging.

[25]  Michael W. L. Chee,et al.  Longitudinal brain structure and cognitive changes over 8 years in an East Asian cohort , 2017, NeuroImage.

[26]  M. Natasha Rajah,et al.  Prefrontal contributions to domain-general executive control processes during temporal context retrieval , 2008, Neuropsychologia.

[27]  Leslie G. Ungerleider,et al.  The prefrontal cortex and the executive control of attention , 2008, Experimental Brain Research.

[28]  R. Ivry,et al.  The Cerebellum: Adaptive Prediction for Movement and Cognition , 2017, Trends in Cognitive Sciences.

[29]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[30]  Ralph Weidner,et al.  Neural Mechanisms of Attentional Reorienting in Three-Dimensional Space , 2012, The Journal of Neuroscience.

[31]  Fabrice Crivello,et al.  Age- and sex-related effects on the neuroanatomy of healthy elderly , 2005, NeuroImage.

[32]  A. Karmiloff-Smith,et al.  The importance of understanding individual differences in Down syndrome , 2016, F1000Research.

[33]  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.

[34]  Osamu Abe,et al.  Aging in the CNS: Comparison of gray/white matter volume and diffusion tensor data , 2008, Neurobiology of Aging.

[35]  M. Andersson,et al.  Longitudinal evidence for diminished frontal cortex function in aging , 2010, Proceedings of the National Academy of Sciences.

[36]  Michael D. Greicius,et al.  Distinct Cerebellar Contributions to Intrinsic Connectivity Networks , 2009, NeuroImage.

[37]  Annette Karmiloff-Smith,et al.  An alternative to domain-general or domain-specific frameworks for theorizing about human evolution and ontogenesis. , 2015, AIMS neuroscience.

[38]  P. Satz Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. , 1993 .

[39]  J. Billard,et al.  Mechanisms underlying the neuroprotective effect of brain reserve against late life depression , 2015, Journal of Neural Transmission.

[40]  Jörn Diedrichsen,et al.  Surface-Based Display of Volume-Averaged Cerebellar Imaging Data , 2015, PloS one.

[41]  Natasha M. Maurits,et al.  Brain mechanisms underlying the effects of aging on different aspects of selective attention , 2014, NeuroImage.

[42]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[43]  M. Seghier The Angular Gyrus , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[45]  Evelina Fedorenko The role of domain-general cognitive control in language comprehension , 2014, Front. Psychol..

[46]  O. Martinaud,et al.  La BREF, une batterie rapide d’évaluation frontale , 2005 .

[47]  Y. Stern,et al.  Cognitive reserve , 2009, Neuropsychologia.

[48]  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.

[49]  Evelina eFedorenko The role of domain-general cognitive control in language comprehension , 2014 .

[50]  R. D. Whitman,et al.  Executive functioning and lateralized semantic priming in older adults , 2016 .

[51]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[52]  Fabienne Collette,et al.  Fonctionnement exécutif et réseaux cérébraux , 2014, Revue de neuropsychologie.

[53]  D. Wechsler Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[54]  C. Weiller,et al.  Correct and erroneous picture naming responses in healthy subjects , 2009, Neuroscience Letters.

[55]  Catherine J. Stoodley,et al.  The Cerebellum and Cognition: Evidence from Functional Imaging Studies , 2011, The Cerebellum.

[56]  E. Luders,et al.  Voxel-Based Morphometry , 2015 .

[57]  Y. Stern What is cognitive reserve? Theory and research application of the reserve concept , 2002, Journal of the International Neuropsychological Society.

[58]  Jörn Diedrichsen,et al.  A spatially unbiased atlas template of the human cerebellum , 2006, NeuroImage.

[59]  L. Nyberg,et al.  Memory aging and brain maintenance , 2012, Trends in Cognitive Sciences.

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

[61]  T. Tombaugh Trail Making Test A and B: normative data stratified by age and education. , 2004, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[62]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

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

[64]  J. Poitrenaud,et al.  Standardisation et étalonnage français du Mini Mental State (MMS) version GRÉCO , 2003 .

[65]  M. Rajah,et al.  Age-related changes in prefrontal cortex activity are associated with behavioural deficits in both temporal and spatial context memory retrieval in older adults , 2010, Cortex.

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

[67]  C. Caltagirone,et al.  The Neuroprotective Effects of Experience on Cognitive Functions: Evidence from Animal Studies on the Neurobiological Bases of Brain Reserve , 2017, Neuroscience.

[68]  W. Perlstein,et al.  Age-related changes in word retrieval: Role of bilateral frontal and subcortical networks , 2008, Neurobiology of Aging.

[69]  Miguel Á Araque-Caballero,et al.  Resting-State Connectivity of the Left Frontal Cortex to the Default Mode and Dorsal Attention Network Supports Reserve in Mild Cognitive Impairment , 2017, Front. Aging Neurosci..

[70]  B. Dubois,et al.  ["The 5 words": a simple and sensitive test for the diagnosis of Alzheimer's disease]. , 2002, Presse medicale.

[71]  Ulman Lindenberger,et al.  Does variability in cognitive performance correlate with frontal brain volume? , 2013, NeuroImage.

[72]  Lorraine K. Tyler,et al.  Word Retrieval Failures in Old Age: The Relationship between Structure and Function , 2010, Journal of Cognitive Neuroscience.

[73]  Adam J. Woods,et al.  Frontal Structural Neural Correlates of Working Memory Performance in Older Adults , 2017, Front. Aging Neurosci..

[74]  Robert C. Welsh,et al.  Aging and the Neural Correlates of Successful Picture Encoding: Frontal Activations Compensate for Decreased Medial-Temporal Activity , 2005, Journal of Cognitive Neuroscience.

[75]  Pietro Pietrini,et al.  Regional network of magnetic resonance imaging gray matter volume in healthy aging , 2006, Neuroreport.

[76]  Alexander N. W. Taylor,et al.  Left Frontal Hub Connectivity during Memory Performance Supports Reserve in Aging and Mild Cognitive Impairment , 2017, Journal of Alzheimer's disease : JAD.

[77]  R. Snaith,et al.  The Hospital Anxiety and Depression Scale , 1983 .

[78]  Luigi Ferrucci,et al.  Association of executive function and performance of dual-task physical tests among older adults: analyses from the InChianti study. , 2006, Age and ageing.

[79]  Ikuko Mukai,et al.  A role of right middle frontal gyrus in reorienting of attention: a case study , 2015, Front. Syst. Neurosci..

[80]  L. Nyberg,et al.  Brain Characteristics of Individuals Resisting Age-Related Cognitive Decline over Two Decades , 2013, The Journal of Neuroscience.

[81]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[82]  L. Bherer,et al.  Le déclin des fonctions exécutives au cours du vieillissement normal, dans la maladie d’Alzheimer et dans la démence frontotemporale , 2004 .

[83]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

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

[85]  Alexa M. Morcom,et al.  Neural Reorganization and Compensation in Aging , 2015, Journal of Cognitive Neuroscience.

[86]  Joseph T. Gwin,et al.  Motor control and aging: Links to age-related brain structural, functional, and biochemical effects , 2010, Neuroscience & Biobehavioral Reviews.

[87]  Kara D. Federmeier,et al.  Event-related potentials reveal the effects of aging on meaning selection and revision. , 2010, Psychophysiology.

[88]  R. Buckner The Cerebellum and Cognitive Function: 25 Years of Insight from Anatomy and Neuroimaging , 2013, Neuron.

[89]  R. Laboissière,et al.  Behavioral evidence for a differential modulation of semantic processing and lexical production by aging: a full linear mixed-effects modeling approach , 2018, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[90]  M. Poncelet,et al.  Changes in Naming and Semantic Abilities With Aging From 50 to 90 years , 2012, Journal of the International Neuropsychological Society.

[91]  A. Wingfield,et al.  Language and the aging brain: patterns of neural compensation revealed by functional brain imaging. , 2006, Journal of neurophysiology.

[92]  D. Cardebat,et al.  Standardisation d'un test de denomination orale : controle des effects de l'age, du sexe et du niveau de scolarite chez des sujets adultes normaux , 1991 .

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