Resting-state slow wave power, healthy aging and cognitive performance

Cognitive functions and spontaneous neural activity show significant changes over the life-span, but the interrelations between age, cognition and resting-state brain oscillations are not well understood. Here, we assessed performance on the Trail Making Test and resting-state magnetoencephalographic (MEG) recordings from 53 healthy adults (18–89 years old) to investigate associations between age-dependent changes in spontaneous oscillatory activity and cognitive performance. Results show that healthy aging is accompanied by a marked and linear decrease of resting-state activity in the slow frequency range (0.5–6.5 Hz). The effects of slow wave power on cognitive performance were expressed as interactions with age: For older (>54 years), but not younger participants, enhanced delta and theta power in temporal and central regions was positively associated with perceptual speed and executive functioning. Consistent with previous work, these findings substantiate further the important role of slow wave oscillations in neurocognitive function during healthy aging.

[1]  S. Rossi,et al.  Clinical neurophysiology of aging brain: From normal aging to neurodegeneration , 2007, Progress in Neurobiology.

[2]  Th R Knösche,et al.  Transformation of Whole-Head MEG Recordings Between Different Sensor Positions / Transformation von Ganzkopf-MEG-Messungen zwischen verschiedenen Sensorpositionen , 2002, Biomedizinische Technik. Biomedical engineering.

[3]  Kaj Blennow,et al.  Slowing of EEG correlates with CSF biomarkers and reduced cognitive speed in elderly with normal cognition over 4 years , 2010, Neurobiology of Aging.

[4]  P. Adank,et al.  Comprehension of a novel accent by young and older listeners. , 2010, Psychology and aging.

[5]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[6]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

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

[8]  Simon Finnigan,et al.  Theta power is reduced in healthy cognitive aging. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  Stephan Kolassa,et al.  Changes in cortical slow wave activity in healthy aging , 2011, Brain Imaging and Behavior.

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

[11]  H. Akaike.  INFORMATION THEORY AS AN EXTENSION OF THE MAXIMUM LIKELIHOOD , 1973 .

[12]  E Pellouchoud,et al.  Neurophysiological signals of working memory in normal aging. , 2001, Brain research. Cognitive brain research.

[13]  H. Gertz,et al.  Does the Hippocampal Atrophy Correlate With the Cortical Theta Power in Elderly Subjects With a Range of Cognitive Impairment? , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[15]  E. R. John,et al.  Prediction of longitudinal cognitive decline in normal elderly with subjective complaints using electrophysiological imaging , 2006, Neurobiology of Aging.

[16]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[17]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[18]  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.

[19]  E. Gordon,et al.  Spontaneous alpha peak frequency predicts working memory performance across the age span. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[20]  P. Rossini,et al.  Sources of cortical rhythms in adults during physiological aging: A multicentric EEG study , 2006, Human brain mapping.

[21]  Task-related brain oscillations in normal aging , 2012 .

[22]  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.

[23]  J. Lépine,et al.  Mini International Neuropsychiatric Interview , 2013 .

[24]  Kathy A. Low,et al.  Different slopes for different folks: alpha and delta EEG power predict subsequent video game learning rate and improvements in cognitive control tasks. , 2012, Psychophysiology.

[25]  L. Nyberg,et al.  Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues , 2010, Neuroscience & Biobehavioral Reviews.

[26]  M Ackenheil,et al.  Deutsche Fassung des Mini-International Neuropsychiatric Interview , 1999 .

[27]  T. Salthouse.  When does age-related cognitive decline begin? , 2009, Neurobiology of Aging.

[28]  Menno P. Witter,et al.  A pathophysiological framework of hippocampal dysfunction in ageing and disease , 2011, Nature Reviews Neuroscience.

[29]  Simon Finnigan,et al.  Resting EEG theta power correlates with cognitive performance in healthy older adults. , 2011, Psychophysiology.

[30]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

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

[32]  K. Meador,et al.  Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. , 2010, Cerebral cortex.

[33]  C. Stam,et al.  Age Distribution of MEG Spontaneous Theta Activity in Healthy Subjects , 2005, Brain Topography.

[34]  K Warner Schaie,et al.  The Seattle Longitudinal Study: Relationship Between Personality and Cognition , 2004, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[35]  G. Bartzokis,et al.  Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. , 2001, Archives of general psychiatry.

[36]  Yee Lee Shing,et al.  Aging Neuroscience , 2022 .

[37]  J. Gabrieli,et al.  Insights into the ageing mind: a view from cognitive neuroscience , 2004, Nature Reviews Neuroscience.

[38]  Camarin E. Rolle,et al.  Video game training enhances cognitive control in older adults , 2013, Nature.

[39]  Bharath Chandrasekaran,et al.  Dual systems of speech category learning across the lifespan. , 2013, Psychology and aging.

[40]  B. Rockstroh,et al.  Focal temporoparietal slow activity in Alzheimer’s disease revealed by magnetoencephalography , 2002, Biological Psychiatry.

[41]  T. Elbert,et al.  Development of large-scale functional networks over the lifespan , 2012, Neurobiology of Aging.

[42]  R. Nigbur,et al.  Theta power as a marker for cognitive interference , 2011, Clinical Neurophysiology.

[43]  David Poeppel,et al.  Cortical oscillations and speech processing: emerging computational principles and operations , 2012, Nature Neuroscience.

[44]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[45]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[46]  F Kruggel,et al.  Correlation Between Cortical &thgr; Activity and Hippocampal Volumes in Health, Mild Cognitive Impairment, and Mild Dementia , 2001, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[47]  Toshiaki Imada,et al.  Theta brain rhythms index perceptual narrowing in infant speech perception , 2013, Front. Psychol..

[48]  H. Soininen,et al.  Aging and spectral analysis of EEG in normal subjects: a link to memory and CSF AChE , 1992, Acta neurologica Scandinavica.

[49]  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.

[50]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

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

[52]  F. Barceló,et al.  Construct validity of the Trail Making Test: Role of task-switching, working memory, inhibition/interference control, and visuomotor abilities , 2009, Journal of the International Neuropsychological Society.

[53]  R. Mohs,et al.  Consortium to establish a registry for Alzheimer's disease (CERAD) clinical and neuropsychological assessment of Alzheimer's disease. , 2002, Psychopharmacology bulletin.

[54]  Marco Congedo,et al.  Neurofeedback Improves Executive Functioning in Children with Autism Spectrum Disorders. , 2009 .

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

[56]  Ehren L. Newman,et al.  Human θ Oscillations Related to Sensorimotor Integration and Spatial Learning , 2003, The Journal of Neuroscience.