Specific EEG Changes Associated with Atrophy of Hippocampus in Subjects with Mild Cognitive Impairment and Alzheimer's Disease

We evaluated the association between hippocampal atrophy and increase of the EEG markers alpha3/alpha2 relative power ratio in mild cognitive impairment (MCI) and Alzheimer's disease patients. Seventy-nine subjects with MCI and 11 patients with AD underwent EEG recording and MRI scan. The MCI group was subdivided in three subgroups according to growing hippocampal atrophy. The groups were characterized by alpha3/alpha2 relative power ratio. In AD patients group mapped hippocampal regions were computed and related with alpha3/alpha2 power ratio. Results show that the increase of alpha3/alpha2 power ratio is correlated with atrophy of hippocampus both in MCI and in Alzheimer's disease patients. This finding confirms the possible diagnostic role of EEG markers as diagnostic and prognostic factors in patient with prodromal and declared Alzheimer's disease.

[1]  P. Scheltens,et al.  Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS–ADRDA criteria , 2007, The Lancet Neurology.

[2]  M. Albert,et al.  Use of brief cognitive tests to identify individuals in the community with clinically diagnosed Alzheimer's disease. , 1991, The International journal of neuroscience.

[3]  J. T. Erichsen,et al.  Hippocampal inputs mediate theta-related plasticity in anterior thalamus , 2011, Neuroscience.

[4]  L. Cahill,et al.  Neurobiological mechanisms of emotionally influenced, long-term memory. , 2000, Progress in brain research.

[5]  P. Rossini,et al.  Hippocampal atrophy and EEG markers in subjects with mild cognitive impairment , 2007, Clinical Neurophysiology.

[6]  Y. Ikegaya,et al.  Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats , 1994, Brain Research.

[7]  J. T. Erichsen,et al.  Hippocampal–anterior thalamic pathways for memory: uncovering a network of direct and indirect actions , 2010, The European journal of neuroscience.

[8]  Rossana Ganzola,et al.  Mapping local hippocampal changes in Alzheimer's disease and normal ageing with MRI at 3 Tesla. , 2008, Brain : a journal of neurology.

[9]  E Capitani,et al.  Raven's coloured progressive matrices: normative values on 305 adult normal controls. , 1987, Functional neurology.

[10]  G. Frisoni,et al.  Medial temporal atrophy but not memory deficit predicts progression to dementia in patients with mild cognitive impairment , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[11]  Andrea Tales,et al.  Abnormal visual search in mild cognitive impairment and Alzheimer’s disease , 2005, Neurocase.

[12]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[13]  Charles DeCarli,et al.  Mild cognitive impairment: prevalence, prognosis, aetiology, and treatment , 2003, The Lancet Neurology.

[14]  Cristina Geroldi,et al.  Increase of theta/gamma and alpha3/alpha2 ratio is associated with amygdalo-hippocampal complex atrophy. , 2009, Journal of Alzheimer's disease : JAD.

[15]  Alan C. Evans,et al.  Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. , 2000, Cerebral cortex.

[16]  Paolo Maria Rossini,et al.  Cerebrovascular disease and hippocampal atrophy are differently linked to functional coupling of brain areas: an EEG coherence study in MCI subjects. , 2008, Journal of Alzheimer's disease : JAD.

[17]  R. Petersen,et al.  Mild Cognitive Impairment: An Overview , 2008, CNS Spectrums.

[18]  F. H. Lopes da Silva,et al.  Alpha rhythms: noise, dynamics and models. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  D. Paré,et al.  Ultrastructural organization of medial prefrontal inputs to the rhinal cortices , 2006, The European journal of neuroscience.

[20]  Yaakov Stern,et al.  Hippocampal subregions differentially associate with standardized memory tests , 2010, Hippocampus.

[21]  Paul M. Thompson,et al.  In vivo neuropathology of the hippocampal formation in AD: A radial mapping MR-based study , 2006, NeuroImage.

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

[23]  J. Morris,et al.  Current concepts in mild cognitive impairment. , 2001, Archives of neurology.

[24]  Dawn R. Collins,et al.  Amygdala oscillations and the consolidation of emotional memories , 2002, Trends in Cognitive Sciences.

[25]  A. Pfeffer,et al.  Magnetic Resonance Imaging-Based Hippocampal Volumetry in Patients with Dementia of the Alzheimer Type , 1999, Dementia and Geriatric Cognitive Disorders.

[26]  Manuel Schabus,et al.  Theta coupling in the human electroencephalogram during a working memory task , 2004, Neuroscience Letters.

[27]  P. Caffarra,et al.  Rey-Osterrieth complex figure: normative values in an Italian population sample , 2002, Neurological Sciences.

[28]  M. Lawton,et al.  Assessment of older people: self-maintaining and instrumental activities of daily living. , 1969, The Gerontologist.

[29]  G. Richter-Levin,et al.  Priming stimulation in the basolateral amygdala modulates synaptic plasticity in the rat dentate gyrus , 1999, Neuroscience Letters.

[30]  P. Ryvlin,et al.  Evoked potential study of hippocampal efferent projections in the human brain , 2011, Clinical Neurophysiology.

[31]  Simulated Mossy Fiber Associated Feedforward Circuit Functioning as a Highpass Filter , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[32]  R. Wurtman,et al.  Phentermine and other monoamine-oxidase inhibitors may increase plasma serotonin when given with fenfluramines , 1999, The Lancet.

[33]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Jack,et al.  Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease , 1997, Neurology.

[35]  D. Schaid,et al.  Apolipoprotein E status as a predictor of the development of Alzheimer's disease in memory-impaired individuals. , 1995, JAMA.

[36]  A. Papanicolaou,et al.  The hippocampus and memory of verbal and pictorial material. , 2002, Learning & memory.

[37]  P. Johannsen,et al.  Cortical Responses to Sustained and Divided Attention in Alzheimer's Disease , 1999, NeuroImage.

[38]  J. Wegiel,et al.  MRI of entorhinal cortex in mild Alzheimer's disease , 1999, The Lancet.

[39]  Hilkka Soininen,et al.  Hippocampus in Alzheimer’s disease: a 3-year follow-up MRI study , 2000, Biological Psychiatry.

[40]  D. Paré,et al.  Neuronal Correlates of Fear in the Lateral Amygdala: Multiple Extracellular Recordings in Conscious Cats , 2000, The Journal of Neuroscience.

[41]  A. Toga,et al.  Cortical variability and asymmetry in normal aging and Alzheimer's disease. , 1998, Cerebral cortex.

[42]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[43]  A. Toga,et al.  High-Resolution Random Mesh Algorithms for Creating a Probabilistic 3D Surface Atlas of the Human Brain , 1996, NeuroImage.

[44]  Paul M. Thompson,et al.  Regional specificity of hippocampal volume reductions in first-episode schizophrenia , 2004, NeuroImage.

[45]  R. Sperling,et al.  Functional MRI Studies of Associative Encoding in Normal Aging, Mild Cognitive Impairment, and Alzheimer's Disease , 2007, Annals of the New York Academy of Sciences.

[46]  K. Shulman Clock‐drawing: is it the ideal cognitive screening test? , 2000, International journal of geriatric psychiatry.

[47]  Paul M. Thompson,et al.  In vivo mapping of incremental cortical atrophy from incipient to overt Alzheimer’s disease , 2009, Journal of Neurology.

[48]  T Seidenbecher,et al.  Reinforcement of Early Long-Term Potentiation (Early-LTP) in Dentate Gyrus by Stimulation of the Basolateral Amygdala: Heterosynaptic Induction Mechanisms of Late-LTP , 2001, The Journal of Neuroscience.

[49]  A. Hofman,et al.  Use of hippocampal and amygdalar volumes on magnetic resonance imaging to predict dementia in cognitively intact elderly people. , 2006, Archives of general psychiatry.

[50]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Daniela Mapelli,et al.  Variability of Trail Making Test, Symbol Digit Test and Line Trait Test in normal people. A normative study taking into account age-dependent decline and sociobiological variables , 2002, Aging clinical and experimental research.

[52]  L. Radloff The CES-D Scale , 1977 .

[53]  Kiralee M. Hayashi,et al.  The topography of grey matter involvement in early and late onset Alzheimer's disease. , 2007, Brain : a journal of neurology.

[54]  N. Nishiyama,et al.  Medial amygdala enhances synaptic transmission and synaptic plasticity in the dentate gyrus of rats in vivo. , 1995, Journal of neurophysiology.

[55]  W. Klimesch,et al.  The interplay between theta and alpha oscillations in the human electroencephalogram reflects the transfer of information between memory systems , 2002, Neuroscience Letters.

[56]  J. Rabe-Jabłońska,et al.  [Affective disorders in the fourth edition of the classification of mental disorders prepared by the American Psychiatric Association -- diagnostic and statistical manual of mental disorders]. , 1993, Psychiatria polska.

[57]  J. D. McGaugh,et al.  Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[58]  György Buzsáki,et al.  Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance , 2007, Proceedings of the National Academy of Sciences.

[59]  R. Petersen,et al.  Aging, Memory, and Mild Cognitive Impairment , 1997, International Psychogeriatrics.

[60]  C. P. Hughes,et al.  A New Clinical Scale for the Staging of Dementia , 1982, British Journal of Psychiatry.

[61]  G. B. Frisoni,et al.  Volumetric Differences in Mapped Hippocampal Regions Correlate with Increase of High Alpha Rhythm in Alzheimer's Disease , 2011, International journal of Alzheimer's disease.

[62]  Claudio Babiloni,et al.  Individual analysis of EEG frequency and band power in mild Alzheimer's disease , 2004, Clinical Neurophysiology.

[63]  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.

[64]  R. Katzman.,et al.  Pathological verification of ischemic score in differentiation of dementias , 1980, Annals of neurology.

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

[66]  Olivier Salvado,et al.  Detecting global and local hippocampal shape changes in Alzheimer's disease using statistical shape models , 2012, NeuroImage.

[67]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[68]  C. Caltagirone,et al.  The Mental Deterioration Battery: Normative Data, Diagnostic Reliability and Qualitative Analyses of Cognitive Impairment , 1996 .

[69]  Henri M. Duvernoy The human hippocampus , 1988 .

[70]  Robert P. Vertes,et al.  Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat , 2006, Neuroscience.

[71]  P. Scheltens,et al.  Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI Working Group of the European Consortium on Alzheimer’s Disease , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[72]  A. Tales,et al.  Abnormal spatial and non-spatial cueing effects in mild cognitive impairment and Alzheimer’s disease , 2005, Neurocase.

[73]  N. Schuff,et al.  Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease , 2001, Journal of neurology, neurosurgery, and psychiatry.