Induced oscillatory responses during the Sternberg's visual memory task in patients with Alzheimer's disease and mild cognitive impairment

In this study we used magnetoencephalography during a modified version of the Sternberg's memory recognition task performed by patients with early Alzheimer's disease (AD), mild cognitive impairment (MCI), and by age-matched healthy controls to identify differences in induced oscillatory responses. For analyses, we focused on the retention period of the working memory task. Multiple-source beamformer and Brain Voyager were used for localization of source-power changes across the cortex and for statistic group analyses, respectively. We found significant differences in oscillatory response during the task, specifically in beta and gamma frequency bands: patients with AD showed reduced beta event-related desynchronization (ERD) in the right central area compared to controls, and reduced gamma ERD in the left prefrontal and medial parietal cortex compared to patients with MCI. Our findings suggest that reduced oscillatory responses over certain brain regions in high frequency bands (i.e., beta, gamma), and especially in the beta band that was significantly different between AD patients and healthy subjects, may represent brain electromagnetic changes underlying visual-object working memory dysfunction in early AD, and a neurophysiological indicator of cognitive decline.

[1]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[2]  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.

[3]  R. Hashimoto,et al.  Working memory abnormalities in chronic interictal epileptic psychosis and schizophrenia revealed by magnetoencephalography , 2010, Epilepsy & Behavior.

[4]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[5]  et al.,et al.  Discrimination between Alzheimer Dementia and Controls by Automated Analysis of Multicenter FDG PET , 2002, NeuroImage.

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

[7]  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.

[8]  S. Sikström,et al.  Aging cognition: from neuromodulation to representation , 2001, Trends in Cognitive Sciences.

[9]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[10]  Blake W. Johnson,et al.  Measurement of brain function in pre-school children using a custom sized whole-head MEG sensor array , 2010, Clinical Neurophysiology.

[11]  本間昭 Alzheimer’s Disease Assessment Scale(ADAS)日本版の作成 , 1992 .

[12]  C. J Stam,et al.  Brain dynamics in theta and alpha frequency bands and working memory performance in humans , 2000, Neuroscience Letters.

[13]  栗本 龍,et al.  Event-related synchronization of alpha activity in early Alzheimer's disease and mild cognitive impairment : an MEG study combining beamformer and group comparison , 2009 .

[14]  Christian Haarala Björnberg,et al.  Brain oscillatory 1–30Hz EEG ERD/ERS responses during the different stages of an auditory memory search task , 2006, Neuroscience Letters.

[15]  T. Ohnishi,et al.  Longitudinal Evaluation of Early Alzheimer's Disease Using Brain Perfusion Spect the Recruitment Was For , 2000 .

[16]  P. Campo,et al.  Medial temporal lobe neuromagnetic hypoactivation and risk for developing cognitive decline in elderly population: A 2-year follow-up study , 2006, Neurobiology of Aging.

[17]  T. Demiralp,et al.  Human EEG gamma oscillations in neuropsychiatric disorders , 2005, Clinical Neurophysiology.

[18]  P. Campo,et al.  Increased biomagnetic activity in the ventral pathway in mild cognitive impairment , 2008, Clinical Neurophysiology.

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

[20]  Matti Laine,et al.  Brain oscillatory responses to an auditory-verbal working memory task in mild cognitive impairment and Alzheimer's disease. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  M. Laine,et al.  Effects of normal aging on event-related desynchronization/synchronization during a memory task in humans , 2004, Neuroscience Letters.

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

[23]  S. Sternberg High-Speed Scanning in Human Memory , 1966, Science.

[24]  M. Hämäläinen Magnetoencephalography: A tool for functional brain imaging , 2005, Brain Topography.

[25]  B. Reisberg,et al.  Mild cognitive impairment , 2005, The Lancet.

[26]  Fernando Maestu,et al.  Increased biomagnetic activity in healthy elderly with subjective memory complaints , 2011, Clinical Neurophysiology.

[27]  P. Barberger‐Gateau,et al.  [Prevalence of dementia and Alzheimer's disease among subjects aged 75 years or over: updated results of the PAQUID cohort]. , 2003, Revue neurologique.

[28]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[29]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[30]  T. Yoshimine,et al.  Post-movement beta rebound abnormality as indicator of mirror neuron system dysfunction in autistic spectrum disorder: An MEG study , 2010, Neuroscience Letters.

[31]  Fernando Maestú,et al.  Functional connectivity in mild cognitive impairment during a memory task: implications for the disconnection hypothesis. , 2010, Journal of Alzheimer's disease : JAD.

[32]  R. Petersen Mild cognitive impairment as a diagnostic entity , 2004, Journal of internal medicine.

[33]  H. Ramaroson,et al.  Prévalence de la démence et de la maladie d'Alzheimer chez les personnes de 75 ans et plus : données réactualisées de la cohorte PAQUID , 2003 .

[34]  Ahmed H. Tewfik,et al.  Classification of schizophrenia with spectro-temporo-spatial MEG patterns in working memory , 2009, Clinical Neurophysiology.

[35]  J. Morris The Clinical Dementia Rating (CDR) , 1993, Neurology.

[36]  Alberto Fernández,et al.  Magnetoencephalographic parietal delta dipole density in mild cognitive impairment: preliminary results of a method to estimate the risk of developing Alzheimer disease. , 2006, Archives of neurology.

[37]  T. Inouye,et al.  Medial prefrontal cortex generates frontal midline theta rhythm. , 1999, Neuroreport.

[38]  G. Barnes,et al.  Language dominance and mapping based on neuromagnetic oscillatory changes: comparison with invasive procedures. , 2010, Journal of neurosurgery.

[39]  M. Manosevitz High-Speed Scanning in Human Memory , .

[40]  C. Pantev,et al.  Cortical oscillatory power changes during auditory oddball task revealed by spatially filtered magnetoencephalography , 2009, Clinical Neurophysiology.

[41]  P. Pasqualetti,et al.  Alpha rhythms in mild dements during visual delayed choice reaction time tasks: A MEG study , 2005, Brain Research Bulletin.

[42]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[43]  石井 良平 Medial prefrontal cortex generates frontal midline theta rhythm , 1999 .

[44]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[45]  M-X Huang,et al.  Commonalities and Differences Among Vectorized Beamformers in Electromagnetic Source Imaging , 2003, Brain Topography.

[46]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[47]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[48]  P. Giannakopoulos,et al.  Working memory load–related electroencephalographic parameters can differentiate progressive from stable mild cognitive impairment , 2007, Neuroscience.

[49]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[50]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[51]  Mirka Pesonen,et al.  Brain oscillatory 4–30 Hz responses during a visual n-back memory task with varying memory load , 2007, Brain Research.

[52]  G Pfurtscheller,et al.  Event-related desynchronization during motor behavior and visual information processing. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[53]  J Arrazola,et al.  Spatio-temporal patterns of brain magnetic activity during a memory task in Alzheimer's disease , 2001, Neuroreport.

[54]  M. Bastiaansen,et al.  Event-related alpha and theta responses in a visuo-spatial working memory task , 2002, Clinical Neurophysiology.

[55]  Toshiki Yoshimine,et al.  Magnetoencephalographic analysis of cortical oscillatory activity in patients with brain tumors: Synthetic aperture magnetometry (SAM) functional imaging of delta band activity , 2007, NeuroImage.

[56]  Yong-Sheng Chen,et al.  Maximum contrast beamformer for electromagnetic mapping of brain activity , 2006, IEEE Transactions on Biomedical Engineering.

[57]  Agnieszka Grabska-Barwińska,et al.  A model of event-related EEG synchronization changes in beta and gamma frequency bands. , 2006, Journal of theoretical biology.