Age-related Shift in Neural Complexity Related to Task Performance and Physical Activity

The human brain undergoes marked structural changes with age including cortical thinning and reduced connectivity because of the degradation of myelin. Although these changes can compromise cognitive function, the brain is able to functionally reorganize to compensate for some of this structural loss. However, there are interesting individual differences in outcome: When comparing individuals of similar age, those who engage in regular physical activity are less affected by the typical age-related decline in cognitive function. This study used multiscale entropy to reveal a shift in the way the brain processes information in older adults that is related to physical activity. Specifically, older adults who were more physically active engaged in more local neural information processing. Interestingly, this shift toward local information processing was also associated with improved executive function performance in older adults, suggesting that physical activity may help to improve aspects of cognitive function in older adults by biasing the neural system toward local information processing. In the face of age-related structural decline, the neural plasticity that is enhanced through physical activity may help older adults maintain cognitive health longer into their lifespan.

[1]  A. Peters,et al.  In aging, is it gray or white? , 2003, The Journal of comparative neurology.

[2]  E. McAuley,et al.  Functional connectivity: A source of variance in the association between cardiorespiratory fitness and cognition? , 2010, Neuropsychologia.

[3]  E. McAuley,et al.  Frontiers in Aging Neuroscience Aging Neuroscience , 2022 .

[4]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[5]  G. Radvansky,et al.  Studies of directed forgetting in older adults. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[6]  F. Gage,et al.  Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus , 1999, Nature Neuroscience.

[7]  Natasa Kovacevic,et al.  Brain signal variability relates to stability of behavior after recovery from diffuse brain injury , 2012, NeuroImage.

[8]  Vasily A. Vakorin,et al.  Variability of Brain Signals Processed Locally Transforms into Higher Connectivity with Brain Development , 2011, Journal of Neuroscience.

[9]  Anthony R. McIntosh,et al.  Functional Embedding Predicts the Variability of Neural Activity , 2011, Front. Syst. Neurosci..

[10]  R. Cabeza,et al.  Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. , 2004, Cerebral cortex.

[11]  Robert A. Bjork,et al.  Positive forgetting: The noninterference of Items intentionally forgotten , 1970 .

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

[13]  Madalena Costa,et al.  Multiscale entropy analysis of biological signals. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Ilana B. Clark,et al.  Physical Fitness and Sociocognitive Engagement are Associated with Different Aspects of Cognition in Older Adults , 2015, Journal of the American Geriatrics Society.

[15]  Christopher Hertzog,et al.  Assessing adult leisure activities: an extension of a self-report activity questionnaire. , 2010, Psychological assessment.

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

[17]  Denise C. Park,et al.  The adaptive brain: aging and neurocognitive scaffolding. , 2009, Annual review of psychology.

[18]  A. Kramer,et al.  Fitness Effects on the Cognitive Function of Older Adults , 2003, Psychological science.

[19]  Charles H Hillman,et al.  Physical activity and cognitive function in a cross-section of younger and older community-dwelling individuals. , 2006, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[20]  David H. Salat,et al.  The Declining Infrastructure of the Aging Brain , 2011, Brain Connect..

[21]  A. McIntosh,et al.  Spatiotemporal analysis of experimental differences in event-related potential data with partial least squares. , 2001, Psychophysiology.

[22]  G. Bartzokis Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease , 2004, Neurobiology of Aging.

[23]  A. McIntosh,et al.  Applications of EEG Neuroimaging Data: Event-related Potentials, Spectral Power, and Multiscale Entropy , 2013, Journal of visualized experiments : JoVE.

[24]  Natasa Kovacevic,et al.  Increased Brain Signal Variability Accompanies Lower Behavioral Variability in Development , 2008, PLoS Comput. Biol..

[25]  Kristin A. Lowry,et al.  Exercise, Fitness, and Neurocognitive Function in Older Adults: The “Selective Improvement” and “Cardiovascular Fitness” Hypotheses , 2008, Annals of behavioral medicine : a publication of the Society of Behavioral Medicine.

[26]  Lynn Hasher,et al.  Language, memory, and aging: Capacity theory and the processing of inferences , 1988 .

[27]  Anthony Randal McIntosh,et al.  A Trade-off between Local and Distributed Information Processing Associated with Remote Episodic versus Semantic Memory , 2014, Journal of Cognitive Neuroscience.

[28]  Kristopher J Preacher,et al.  SPSS and SAS procedures for estimating indirect effects in simple mediation models , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[29]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

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

[31]  M. P. Griffin,et al.  Sample entropy analysis of neonatal heart rate variability. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[32]  Anthony R McIntosh,et al.  Age differences in the association of physical activity, sociocognitive engagement, and TV viewing on face memory. , 2015, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[33]  C. Grady,et al.  The Importance of Being Variable , 2011, The Journal of Neuroscience.

[34]  Mark D'Esposito,et al.  Dissociating Age-related Changes in Cognitive Strategy and Neural Efficiency Using Event- related fMRI , 2005, Cortex.

[35]  A. Kramer,et al.  Be smart, exercise your heart: exercise effects on brain and cognition , 2008, Nature Reviews Neuroscience.

[36]  A. Kramer,et al.  Enrichment Effects on Adult Cognitive Development , 2008, Psychological science in the public interest : a journal of the American Psychological Society.

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

[38]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[39]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[40]  J. Cummings,et al.  The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment , 2005, Journal of the American Geriatrics Society.

[41]  O. Spreen,et al.  Predicting premorbid IQ: A revision of the national adult reading test , 1989 .

[42]  Anthony Randal McIntosh,et al.  Relating brain signal variability to knowledge representation , 2012, NeuroImage.

[43]  Natasa Kovacevic,et al.  Differential Maturation of Brain Signal Complexity in the Human Auditory and Visual System , 2009, Frontiers in human neuroscience.

[44]  G. Zitnik,et al.  Age‐related decline in neurogenesis: Old cells or old environment? , 2002, Journal of neuroscience research.

[45]  Paige E. Scalf,et al.  Cardiovascular fitness, cortical plasticity, and aging. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Vasily A. Vakorin,et al.  Spatiotemporal Dependency of Age-Related Changes in Brain Signal Variability , 2013, Cerebral cortex.

[47]  H. Praag,et al.  Bridging animal and human models of exercise-induced brain plasticity , 2013, Trends in Cognitive Sciences.

[48]  Edward McAuley,et al.  The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: Results of a one‐year exercise intervention , 2013, Human brain mapping.

[49]  Soo Yong Kim,et al.  MULTISCALE ENTROPY ANALYSIS OF EEG FROM PATIENTS UNDER DIFFERENT PATHOLOGICAL CONDITIONS , 2007 .

[50]  C. Cotman,et al.  Exercise: a behavioral intervention to enhance brain health and plasticity , 2002, Trends in Neurosciences.

[51]  Margot J. Taylor,et al.  Brain noise is task dependent and region specific. , 2010, Journal of neurophysiology.