The Relationship of Cognitive Performance and the Theta-Alpha Power Ratio Is Age-Dependent: An EEG Study of Short Term Memory and Reasoning during Task and Resting-State in Healthy Young and Old Adults

Objective: The Theta-Alpha ratio (TAR) is known to differ based upon age and cognitive ability, with pathological electroencephalography (EEG) patterns routinely found within neurodegenerative disorders of older adults. We hypothesized that cognitive ability would predict EEG metrics differently within healthy young and old adults, and that healthy old adults not showing age-expected EEG activity may be more likely to demonstrate cognitive deficits relative to old adults showing these expected changes. Methods: In 216 EEG blocks collected in 16 young and 20 old adults during rest (eyes open, eyes closed) and cognitive tasks (short-term memory [STM]; matrix reasoning [RM; Raven's matrices]), models assessed the contributing roles of cognitive ability, age, and task in predicting the TAR. A general linear mixed-effects regression model was used to model this relationship, including interaction effects to test whether increased cognitive ability predicted TAR differently for young and old adults at rest and during cognitive tasks. Results: The relationship between cognitive ability and the TAR across all blocks showed age-dependency, and cognitive performance at the CZ midline location predicted the TAR measure when accounting for the effect of age (p < 0.05, chi-square test of nested models). Age significantly interacted with STM performance in predicting the TAR (p < 0.05); increases in STM were associated with increased TAR in young adults, but not in old adults. RM showed similar interaction effects with aging and TAR (p < 0.10). Conclusion: EEG correlates of cognitive ability are age-dependent. Adults who did not show age-related EEG changes were more likely to exhibit cognitive deficits than those who showed age-related changes. This suggests that healthy aging should produce moderate changes in Alpha and TAR measures, and the absence of such changes signals impaired cognitive functioning.

[1]  E. Basar,et al.  Review of delta, theta, alpha, beta, and gamma response oscillations in neuropsychiatric disorders. , 2013, Supplements to Clinical neurophysiology.

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

[3]  R. Fariello,et al.  Computer analysis of EEG activity in dementia of the Alzheimer's type and Huntington's disease , 1990, Neurobiology of Aging.

[4]  Davide V. Moretti,et al.  Theta and alpha EEG frequency interplay in subjects with mild cognitive impairment: evidence from EEG, MRI, and SPECT brain modifications , 2015, Front. Aging Neurosci..

[5]  Sacha Jennifer van Albada,et al.  Age trends and sex differences of alpha rhythms including split alpha peaks , 2011, Clinical Neurophysiology.

[6]  D. Salat,et al.  Greater orbital prefrontal volume selectively predicts worse working memory performance in older adults. , 2002, Cerebral cortex.

[7]  Steve Majerus,et al.  The neural correlates of verbal short-term memory in Alzheimer's disease: an fMRI study. , 2009, Brain : a journal of neurology.

[8]  J. Lubar,et al.  Electroencephalographic peak alpha frequency correlates of cognitive traits , 2004, Neuroscience Letters.

[9]  Sergio Machado,et al.  Index of Alpha/Theta Ratio of the Electroencephalogram: A New Marker for Alzheimer’s Disease , 2013, Front. Aging Neurosci..

[10]  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.

[11]  Paco Martorell,et al.  Monetary costs of dementia in the United States. , 2013, The New England journal of medicine.

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

[13]  Ulman Lindenberger,et al.  Individual alpha peak frequency is related to latent factors of general cognitive abilities , 2013, NeuroImage.

[14]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

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

[16]  J. Yesavage,et al.  Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. , 1986 .

[17]  Chengbiao Lu,et al.  Relative power and coherence of EEG series are related to amnestic mild cognitive impairment in diabetes , 2014, Front. Aging Neurosci..

[18]  Winfried Schlee,et al.  Resting-state slow wave power, healthy aging and cognitive performance , 2014, Scientific Reports.

[19]  R. Barry,et al.  EEG differences between eyes-closed and eyes-open resting conditions , 2007, Clinical Neurophysiology.

[20]  W. Klimesch EEG-alpha rhythms and memory processes. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  K. Langa,et al.  Prevalence of Dementia in the United States: The Aging, Demographics, and Memory Study , 2007, Neuroepidemiology.

[22]  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.

[23]  O Almkvist,et al.  Quantitative electroencephalography power and coherence in Alzheimer's disease and mild cognitive impairment. , 1996, Dementia.

[24]  Claudio Babiloni,et al.  Hippocampal volume and cortical sources of EEG alpha rhythms in mild cognitive impairment and Alzheimer disease , 2009, NeuroImage.

[25]  Arjen van Ooyen,et al.  Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease , 2009, Proceedings of the National Academy of Sciences.

[26]  A. Nordberg,et al.  Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer’s disease , 2000, Neurobiology of Aging.

[27]  N Burgess,et al.  Recoding, storage, rehearsal and grouping in verbal short-term memory: an fMRI study , 2000, Neuropsychologia.

[28]  N. Maurits,et al.  The Relationship between P3 Amplitude and Working Memory Performance Differs in Young and Older Adults , 2013, PloS one.

[29]  Accounting for age differences on the Wisconsin Card Sorting Test: decreased working memory, not inflexibility. , 2001, Psychology and aging.

[30]  T. Cummins,et al.  Theta oscillations are affected by amnestic mild cognitive impairment and cognitive load. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  J. G. Gilbert,et al.  Patterns of declining memory. , 1971, Journal of gerontology.

[32]  Timothy A. Salthouse,et al.  Working memory as a processing resource in cognitive aging , 1990 .

[33]  George V. Rebec,et al.  A new perspective on behavioral inconsistency and neural noise in aging: compensatory speeding of neural communication , 2012, Frontiers in aging neuroscience.

[34]  Scott B. MacKenzie,et al.  Sources of method bias in social science research and recommendations on how to control it. , 2012, Annual review of psychology.

[35]  R W Neufeld,et al.  Declining of memory functions of normal elderly persons , 2000, Psychiatry and clinical neurosciences.

[36]  G. Tedrus,et al.  EEG Theta and Alpha Reactivity on Opening the Eyes in the Diagnosis of Alzheimer's Disease , 2011, Clinical EEG and neuroscience.

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

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

[39]  R. Goutagny,et al.  Decreased theta power at encoding and cognitive mapping deficits in elderly individuals during a spatial memory task , 2015, Neurobiology of Aging.

[40]  J. Polich,et al.  EEG and ERP assessment of normal aging. , 1997, Electroencephalography and clinical neurophysiology.

[41]  H. Soininen,et al.  Quantitative analysis of occipital EEG in different stages of Alzheimer's disease. , 1985, Electroencephalography and clinical neurophysiology.

[42]  J. Desmond,et al.  Neural Substrates of Fluid Reasoning: An fMRI Study of Neocortical Activation during Performance of the Raven's Progressive Matrices Test , 1997, Cognitive Psychology.

[43]  Saskia Haegens,et al.  Inter- and intra-individual variability in alpha peak frequency , 2014, NeuroImage.

[44]  A. Parkin,et al.  Aging, short-term memory, and frontal dysfunction , 1991, Psychobiology.

[45]  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.