Changes in fitness are associated with changes in hippocampal microstructure and hippocampal volume among older adults

This study investigates the effects of fitness changes on hippocampal microstructure and hippocampal volume. Fifty-two healthy participants aged 59-74years with a sedentary lifestyle were randomly assigned to either of two levels of exercise intensity. Training lasted for six months. Physical fitness, hippocampal volumes, and hippocampal microstructure were measured before and after training. Hippocampal microstructure was assessed by mean diffusivity, which inversely reflects tissue density; hence, mean diffusivity is lower for more densely packed tissue. Mean changes in fitness did not differ reliably across intensity levels of training, so data were collapsed across groups. Multivariate modeling of pretest-posttest differences using structural equation modeling (SEM) revealed that individual differences in latent change were reliable for all three constructs. More positive changes in fitness were associated with more positive changes in tissue density (i.e., more negative changes in mean diffusivity), and more positive changes in tissue density were associated with more positive changes in volume. We conclude that fitness-related changes in hippocampal volume may be brought about by changes in tissue density. The relative contributions of angiogenesis, gliogenesis, and/or neurogenesis to changes in tissue density remain to be identified.

[1]  U. Lindenberger,et al.  Frontiers in Aging Neuroscience Aging Neuroscience Hundred Days of Cognitive Training Enhance Broad Cognitive Abilities in Adulthood: Findings from the Cogito Study Materials and Methods Participants and Procedure , 2022 .

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

[3]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

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

[5]  Hui Chang,et al.  Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats , 2008, Brain Research.

[6]  R. Wing,et al.  Genetic modifiers of cardiorespiratory fitness response to lifestyle intervention. , 2014, Medicine and science in sports and exercise.

[7]  Csaba Nyakas,et al.  Physical exercise leads to rapid adaptations in hippocampal vasculature: Temporal dynamics and relationship to cell proliferation and neurogenesis , 2009, Hippocampus.

[8]  Michael C. Neale,et al.  An Algorithm for the Hierarchical Organization of Path Diagrams and Calculation of Components of Expected Covariance , 2002 .

[9]  C. Hillman,et al.  Physical activity, brain, and cognition , 2015, Current Opinion in Behavioral Sciences.

[10]  E. McAuley,et al.  Exercise training increases size of hippocampus and improves memory , 2011, Proceedings of the National Academy of Sciences.

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

[12]  Nancy W Glynn,et al.  Physical activity predicts microstructural integrity in memory-related networks in very old adults. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[13]  U. Lindenberger,et al.  On the power of multivariate latent growth curve models to detect correlated change. , 2006, Psychological methods.

[14]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.

[15]  David M. Diamond,et al.  The stressed hippocampus, synaptic plasticity and lost memories , 2002, Nature Reviews Neuroscience.

[16]  G. Kempermann New neurons for 'survival of the fittest' , 2012, Nature Reviews Neuroscience.

[17]  J. Mcardle,et al.  Using Multivariate Data to Structure Developmental Change , 2019, Life-Span Developmental Psychology.

[18]  C. Bloor Angiogenesis during exercise and training , 2005, Angiogenesis.

[19]  B. Czéh,et al.  Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: Implications for depression and antidepressant action , 2010, European Neuropsychopharmacology.

[20]  I. Frey,et al.  Freiburger Fragebogen zur körperlichen Aktivität-Entwicklung, Prüfung und Anwendung , 2005, Sozial- und Präventivmedizin.

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

[22]  Ulman Lindenberger,et al.  Evaluating the Power of Latent Growth Curve Models to Detect Individual Differences in Change , 2008 .

[23]  Fred H. Gage,et al.  An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus , 2007, Proceedings of the National Academy of Sciences.

[24]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[25]  Ulman Lindenberger,et al.  Neuroscience and Biobehavioral Reviews Review Structural Brain Plasticity in Adult Learning and Development , 2022 .

[26]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

[27]  R. P. McDonald,et al.  Some algebraic properties of the Reticular Action Model for moment structures. , 1984, The British journal of mathematical and statistical psychology.

[28]  H. Heinze,et al.  Vascular hippocampal plasticity after aerobic exercise in older adults , 2014, Molecular Psychiatry.

[29]  W L Beaver,et al.  Gas exchange theory and the lactic acidosis (anaerobic) threshold. , 1990, Circulation.

[30]  G. Kempermann,et al.  Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli , 2003, The Journal of comparative neurology.

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

[32]  Ulman Lindenberger,et al.  Static and Dynamic Longitudinal Structural Analyses of Cognitive Changes in Old Age , 2003, Gerontology.

[33]  John J. Prindle,et al.  A latent change score analysis of a randomized clinical trial in reasoning training. , 2008, Psychology and aging.

[34]  R. Bammer Basic principles of diffusion-weighted imaging. , 2003, European journal of radiology.

[35]  Martin Styner,et al.  DTIPrep: quality control of diffusion-weighted images , 2014, Front. Neuroinform..

[36]  Nick C. Fox,et al.  A meta-analysis of hippocampal atrophy rates in Alzheimer's disease , 2009, Neurobiology of Aging.

[37]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[38]  Ben Godde,et al.  Not only cardiovascular, but also coordinative exercise increases hippocampal volume in older adults , 2014, Front. Aging Neurosci..

[39]  Hagen B. Huttner,et al.  Dynamics of Hippocampal Neurogenesis in Adult Humans , 2013, Cell.

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

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

[42]  P. Eriksson,et al.  Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. , 2005, Journal of neurophysiology.

[43]  J K Smith,et al.  The Effect of Exercise on the Cerebral Vasculature of Healthy Aged Subjects as Visualized by MR Angiography , 2009, American Journal of Neuroradiology.

[44]  Heidi Johansen-Berg,et al.  The Effects of Aerobic Activity on Brain Structure , 2011, Front. Psychology.

[45]  Brigitte Röder,et al.  Beneficial effects of physical exercise on neuroplasticity and cognition , 2013, Neuroscience & Biobehavioral Reviews.

[46]  L. Bherer,et al.  A Review of the Effects of Physical Activity and Exercise on Cognitive and Brain Functions in Older Adults , 2013, Journal of aging research.