Longitudinal assessment of default-mode brain function in aging

Age-related changes in the default-mode network (DMN) have been identified in prior cross-sectional functional magnetic resonance imaging studies. Here, we investigated longitudinal change in DMN activity and connectivity. Cognitively intact participants (aged 49-79 years at baseline) were scanned twice, with a 6-year interval, while performing an episodic memory task interleaved with a passive control condition. Longitudinal analyses showed that the DMN (control condition > memory task) could be reliably identified at both baseline and follow-up. Differences in the magnitude of task-induced deactivation in posterior DMN regions were observed between baseline and follow-up indicating reduced deactivation in these regions with increasing age. Although no overall longitudinal changes in within-network connectivity were found across the whole sample, individual differences in memory change correlated with change in connectivity. Thus, our results show stability of whole-brain DMN topology and functional connectivity over time in healthy older adults, whereas within-region DMN analyses show reduced deactivation between baseline and follow-up. The current findings provide novel insights into DMN functioning that may assist in identifying brain changes in patient populations, as well as characterizing factors that distinguish between normal and pathologic aging.

[1]  R. Sperling,et al.  Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline , 2010, Neurology.

[2]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[3]  Thad A. Polk,et al.  Human Neuroscience , 2022 .

[4]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[5]  L. Nilsson,et al.  Stressful life events are not associated with the development of dementia , 2013, International Psychogeriatrics.

[6]  Kelly O'Keefe,et al.  Reliability of functional magnetic resonance imaging associative encoding memory paradigms in non‐demented elderly adults , 2011, Human brain mapping.

[7]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

[8]  O. Dietrich,et al.  Test–retest reproducibility of the default‐mode network in healthy individuals , 2009, Human brain mapping.

[9]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[10]  J. Damoiseaux Resting-state fMRI as a biomarker for Alzheimer's disease? , 2012, Alzheimer's Research & Therapy.

[11]  Winfried Schlee,et al.  Top-Down Modulation of the Auditory Steady-State Response in a Task-Switch Paradigm , 2008, Front. Hum. Neurosci..

[12]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[13]  Jonas Persson,et al.  Reduced hippocampal volume in non-demented carriers of the apolipoprotein E ɛ4: Relation to chronological age and recognition memory , 2006, Neuroscience Letters.

[14]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[15]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[16]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[17]  Yong He,et al.  Aging-related changes in the default mode network and its anti-correlated networks: A resting-state fMRI study , 2011, Neuroscience Letters.

[18]  Karen M Rodrigue,et al.  Brain Aging and Its Modifiers , 2007, Annals of the New York Academy of Sciences.

[19]  L. Nyberg,et al.  Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. , 2005, Psychology and aging.

[20]  V. Calhoun,et al.  Interrater and intermethod reliability of default mode network selection , 2009, Human brain mapping.

[21]  Naftali Raz,et al.  A Systems Approach to the Aging Brain: Neuroanatomic Changes, Their Modifiers, and Cognitive Correlates , 2009 .

[22]  Vince D Calhoun,et al.  Resting state and task‐induced deactivation: A methodological comparison in patients with schizophrenia and healthy controls , 2009, Human brain mapping.

[23]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Anthony Randal McIntosh,et al.  Age-related Changes in Brain Activity across the Adult Lifespan , 2006, Journal of Cognitive Neuroscience.

[26]  Jonas Persson,et al.  Reduced functional brain activity response in cognitively intact apolipoprotein E ε4 carriers , 2006 .

[27]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[28]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[29]  Peter Fransson,et al.  Assessing the Influence of Different ROI Selection Strategies on Functional Connectivity Analyses of fMRI Data Acquired During Steady-State Conditions , 2011, PloS one.

[30]  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.

[31]  J. Callicott,et al.  Age-related alterations in default mode network: Impact on working memory performance , 2010, Neurobiology of Aging.

[32]  Thomas R. Barrick,et al.  White matter structural decline in normal ageing: A prospective longitudinal study using tract-based spatial statistics , 2010, NeuroImage.

[33]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[34]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[35]  R. L. Cohen,et al.  On the generality of some memory laws , 1981 .

[36]  David T. Jones,et al.  Age-related changes in the default mode network are more advanced in Alzheimer disease , 2011, Neurology.

[37]  Lourens J. Waldorp,et al.  Functional connectivity analysis of fMRI data using parameterized regions-of-interest , 2011, NeuroImage.

[38]  G. Chételat,et al.  Age effect on the default mode network, inner thoughts, and cognitive abilities , 2013, Neurobiology of Aging.

[39]  J. Morris,et al.  Functional deactivations: Change with age and dementia of the Alzheimer type , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[41]  Jonas Persson,et al.  Longitudinal structure-function correlates in elderly reveal MTL dysfunction with cognitive decline. , 2012, Cerebral cortex.

[42]  V. Calhoun,et al.  Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks , 2008, Human brain mapping.

[43]  Kelly O'Keefe,et al.  Evidence of Altered Posteromedial Cortical fMRI Activity in Subjects at Risk for Alzheimer Disease , 2010, Alzheimer disease and associated disorders.

[44]  Jonas Persson,et al.  Structure-function correlates of cognitive decline in aging. , 2006, Cerebral cortex.

[45]  Abraham Z Snyder,et al.  Reliability of functional localization using fMRI , 2003, NeuroImage.

[46]  L. Nyberg,et al.  Altered deactivation in individuals with genetic risk for Alzheimer's disease , 2008, Neuropsychologia.

[47]  G. Busatto,et al.  Resting-state functional connectivity in normal brain aging , 2013, Neuroscience & Biobehavioral Reviews.

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

[49]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[50]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[51]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[52]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[53]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[54]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[55]  Jeroen van der Grond,et al.  Imaging the default mode network in aging and dementia. , 2012, Biochimica et biophysica acta.

[56]  Richard B. Buxton,et al.  Resting-state BOLD networks versus task-associated functional MRI for distinguishing Alzheimer's disease risk groups , 2009, NeuroImage.

[57]  R. Sperling,et al.  Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation , 2008, Proceedings of the National Academy of Sciences.

[58]  S. M. Resnick,et al.  Stability of Default-Mode Network Activity in the Aging Brain , 2009, Brain Imaging and Behavior.

[59]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[60]  L. Nyberg,et al.  Betula: A Prospective Cohort Study on Memory, Health and Aging , 2004 .

[61]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[62]  James K. Nelson,et al.  Age Differences in Deactivation: A Link to Cognitive Control? , 2007, Journal of Cognitive Neuroscience.