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      Classification of Healthy Subjects and Alzheimer's Disease Patients with Dementia from Cortical Sources of Resting State EEG Rhythms: A Study Using Artificial Neural Networks

      research-article
      1 , 2 ,   2 , 3 , 4 , 2 , 2 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 11 , 12 , 13 , 14 , 14 , 4 , 11 , 10 , 10 , 12 , 15 , 16 , 16 , 16 , 5 , 17 , 18 , 3 , 4
      Frontiers in Neuroscience
      Frontiers Media S.A.
      Alzheimer's disease (AD), electroencephalography (EEG), exact low-resolution brain electromagnetic tomography (eLORETA), linear lagged connectivity, artificial neural networks (ANNs)

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          Abstract

          Previous evidence showed a 75.5% best accuracy in the classification of 120 Alzheimer's disease (AD) patients with dementia and 100 matched normal elderly (Nold) subjects based on cortical source current density and linear lagged connectivity estimated by eLORETA freeware from resting state eyes-closed electroencephalographic (rsEEG) rhythms (Babiloni et al., 2016a). Specifically, that accuracy was reached using the ratio between occipital delta and alpha1 current density for a linear univariate classifier (receiver operating characteristic curves). Here we tested an innovative approach based on an artificial neural network (ANN) classifier from the same database of rsEEG markers. Frequency bands of interest were delta (2–4 Hz), theta (4–8 Hz Hz), alpha1 (8–10.5 Hz), and alpha2 (10.5–13 Hz). ANN classification showed an accuracy of 77% using the most 4 discriminative rsEEG markers of source current density (parietal theta/alpha 1, temporal theta/alpha 1, occipital theta/alpha 1, and occipital delta/alpha 1). It also showed an accuracy of 72% using the most 4 discriminative rsEEG markers of source lagged linear connectivity (inter-hemispherical occipital delta/alpha 2, intra-hemispherical right parietal-limbic alpha 1, intra-hemispherical left occipital-temporal theta/alpha 1, intra-hemispherical right occipital-temporal theta/alpha 1). With these 8 markers combined, an accuracy of at least 76% was reached. Interestingly, this accuracy based on 8 (linear) rsEEG markers as inputs to ANN was similar to that obtained with a single rsEEG marker (Babiloni et al., 2016a), thus unveiling their information redundancy for classification purposes. In future AD studies, inputs to ANNs should include other classes of independent linear (i.e., directed transfer function) and non-linear (i.e., entropy) rsEEG markers to improve the classification.

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          Development and validation of a geriatric depression screening scale: a preliminary report.

          A new Geriatric Depression Scale (GDS) designed specifically for rating depression in the elderly was tested for reliability and validity and compared with the Hamilton Rating Scale for Depression (HRS-D) and the Zung Self-Rating Depression Scale (SDS). In constructing the GDS a 100-item questionnaire was administered to normal and severely depressed subjects. The 30 questions most highly correlated with the total scores were then selected and readministered to new groups of elderly subjects. These subjects were classified as normal, mildly depressed or severely depressed on the basis of Research Diagnostic Criteria (RDC) for depression. The GDS, HRS-D and SDS were all found to be internally consistent measures, and each of the scales was correlated with the subject's number of RDC symptoms. However, the GDS and the HRS-D were significantly better correlated with RDC symptoms than was the SDS. The authors suggest that the GDS represents a reliable and valid self-rating depression screening scale for elderly populations.
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            EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis.

            Evidence is presented that EEG oscillations in the alpha and theta band reflect cognitive and memory performance in particular. Good performance is related to two types of EEG phenomena (i) a tonic increase in alpha but a decrease in theta power, and (ii) a large phasic (event-related) decrease in alpha but increase in theta, depending on the type of memory demands. Because alpha frequency shows large interindividual differences which are related to age and memory performance, this double dissociation between alpha vs. theta and tonic vs. phasic changes can be observed only if fixed frequency bands are abandoned. It is suggested to adjust the frequency windows of alpha and theta for each subject by using individual alpha frequency as an anchor point. Based on this procedure, a consistent interpretation of a variety of findings is made possible. As an example, in a similar way as brain volume does, upper alpha power increases (but theta power decreases) from early childhood to adulthood, whereas the opposite holds true for the late part of the lifespan. Alpha power is lowered and theta power enhanced in subjects with a variety of different neurological disorders. Furthermore, after sustained wakefulness and during the transition from waking to sleeping when the ability to respond to external stimuli ceases, upper alpha power decreases, whereas theta increases. Event-related changes indicate that the extent of upper alpha desynchronization is positively correlated with (semantic) long-term memory performance, whereas theta synchronization is positively correlated with the ability to encode new information. The reviewed findings are interpreted on the basis of brain oscillations. It is suggested that the encoding of new information is reflected by theta oscillations in hippocampo-cortical feedback loops, whereas search and retrieval processes in (semantic) long-term memory are reflected by upper alpha oscillations in thalamo-cortical feedback loops. Copyright 1999 Elsevier Science B.V.
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              Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain.

              This paper presents a new method for localizing the electric activity in the brain based on multichannel surface EEG recordings. In contrast to the models presented up to now the new method does not assume a limited number of dipolar point sources nor a distribution on a given known surface, but directly computes a current distribution throughout the full brain volume. In order to find a unique solution for the 3-dimensional distribution among the infinite set of different possible solutions, the method assumes that neighboring neurons are simultaneously and synchronously activated. The basic assumption rests on evidence from single cell recordings in the brain that demonstrates strong synchronization of adjacent neurons. In view of this physiological consideration the computational task is to select the smoothest of all possible 3-dimensional current distributions, a task that is a common procedure in generalized signal processing. The result is a true 3-dimensional tomography with the characteristic that localization is preserved with a certain amount of dispersion, i.e., it has a relatively low spatial resolution. The new method, which we call Low Resolution Electromagnetic Tomography (LORETA) is illustrated with two different sets of evoked potential data, the first showing the tomography of the P100 component to checkerboard stimulation of the left, right, upper and lower hemiretina, and the second showing the results for the auditory N100 component and the two cognitive components CNV and P300. A direct comparison of the tomography results with those obtained from fitting one and two dipoles illustrates that the new method provides physiologically meaningful results while dipolar solutions fail in many situations. In the case of the cognitive components, the method offers new hypotheses on the location of higher cognitive functions in the brain.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                26 January 2017
                2016
                : 10
                : 604
                Affiliations
                [1] 1Department of Clinical and Experimental Medicine, University of Foggia Foggia, Italy
                [2] 2Department of Electrical and Information Engineering, Polytechnic of Bari Bari, Italy
                [3] 3Department of Physiology and Pharmacology “Vittorio Erspamer”, University of Rome “La Sapienza” Rome, Italy
                [4] 4Department of Neuroscience, IRCCS San Raffaele Pisana Rome, Italy
                [5] 5Department of Integrated Imaging, IRCCS Istituto di Ricerca Diagnostica e Nucleare Napoli, Italy
                [6] 6Department of Motor Sciences and Healthiness, University of Naples Parthenope Naples, Italy
                [7] 7Department of Neurology, IRCCS Oasi Institute for Research on Mental Retardation and Brain Aging Enna, Italy
                [8] 8Clinical Neurology Unit, Department of Neuroscience, University of Genoa and IRCCS Azienda Ospedaliera Universitaria San Martino-IST Genoa, Italy
                [9] 9Dipartimento Emergenza e Trapianti d'Organi, University of Bari Bari, Italy
                [10] 10Unit of Neurodegenerative Diseases, Department of Clinical Research in Neurology, University of Bari “Aldo Moro”, Pia Fondazione Cardinale G. Panico Lecce, Italy
                [11] 11Department of Clinical Research in Neurology, University of Bari “Aldo Moro”, Pia Fondazione Cardinale G. Panico Lecce, Italy
                [12] 12Department of Basic Medical Sciences, Neurosciences and Sense Organs, University of Bari “Aldo Moro” Bari, Italy
                [13] 13Department of Imaging–Division of Radiology, Hospital “Di Venere” Bari, Italy
                [14] 14Division of Neuroradiology, “F. Ferrari” Hospital Lecce, Italy
                [15] 15Center for Neuropsychological Research, Institute of Neurology of the Policlinico Gemelli/Catholic University of Rome Italy
                [16] 16Department of Neuroscience, Mental Health and Sensory Organs, University of Rome “La Sapienza” Rome, Italy
                [17] 17Laboratory of Epidemiology, Neuroimaging and Telemedicine, IRCCS Centro “S. Giovanni di Dio-F.B.F.” Brescia, Italy
                [18] 18Memory Clinic and LANVIE–Laboratory of Neuroimaging of Aging, University Hospitals and University of Geneva Geneva, Switzerland
                Author notes

                Edited by: Nathalie A. Compagnone, Innovative Concept in Drug Development, France

                Reviewed by: Todor Vassilev Gerdjikov, University of Leicester, UK; Emmanuel Chigozie Ifeachor, Plymouth University, UK

                *Correspondence: Claudio Babiloni claudio.babiloni@ 123456uniroma1.it

                This article was submitted to Neuropharmacology, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2016.00604
                5266711
                28184183
                ee912e62-652b-43ba-8a50-96f4bbc5af5b
                Copyright © 2017 Triggiani, Bevilacqua, Brunetti, Lizio, Tattoli, Cassano, Soricelli, Ferri, Nobili, Gesualdo, Barulli, Tortelli, Cardinali, Giannini, Spagnolo, Armenise, Stocchi, Buenza, Scianatico, Logroscino, Lacidogna, Orzi, Buttinelli, Giubilei, Del Percio, Frisoni and Babiloni.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 13 June 2016
                : 19 December 2016
                Page count
                Figures: 3, Tables: 4, Equations: 1, References: 86, Pages: 13, Words: 10830
                Funding
                Funded by: Ministero dell'Istruzione, dell'Università e della Ricerca 10.13039/501100003407
                Funded by: Ministero della Salute 10.13039/501100003196
                Categories
                Neuroscience
                Original Research

                Neurosciences
                alzheimer's disease (ad),electroencephalography (eeg),exact low-resolution brain electromagnetic tomography (eloreta),linear lagged connectivity,artificial neural networks (anns)

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