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Abnormal cortical neural synchronization mechanisms in quiet wakefulness are related to motor deficits, cognitive symptoms, and visual hallucinations in Parkinson's disease patients: an electroencephalographic study
(Elsevier Science Inc., 2020) Babiloni, Claudio; Pascarelli, Maria Teresa; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Rizzo, Marco; Ferri, Raffaele; Soricelli, Andrea; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Salvetti, Marco; Cipollini, Virginia; Bonanni, Laura; Franciotti, Raffaella; Onofrj, Marco; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Aarsland, Dag; Parnetti, Lucilla; Farotti, Lucia; Marizzoni, Moira; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Yener, Görsev; Emek-Savaş, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; McKeith, Ian; Stocchi, Fabrizio; Vacca, Laura; Hampel, Harald; Frisoni, Giovanni B.; De Pandis, Maria Francesca; Del Percio, Claudio
Compared with Alzheimer's disease (AD), Parkinson's disease (PD) shows peculiar clinical manifestations related to vigilance (i.e., executive cognitive deficits and visual hallucinations) that may be reflected in resting-state electroencephalographic rhythms. To test this hypothesis, clinical and resting-state electroencephalographic rhythms in age-, sex-, and education-matched PD patients (N = 136) and Alzheimer's disease patients (AD, N = 85), and healthy older participants (Nold, N = 65), were available from an international archive. Electroencephalographic sources were estimated by eLORETA software. The results are as follows: (1) compared to the Nold participants, the AD and PD patients showed higher widespread delta source activities (PD > AD) and lower posterior alpha source activities (AD > PD); (2) the PD patients with the most pronounced motor deficits exhibited very low alpha source activities in widespread cortical regions; (3) the PD patients with the strongest cognitive deficits showed higher alpha source activities in widespread cortical regions; and (4) compared to the PD patients without visual hallucinations, those with visual hallucinations were characterized by higher posterior alpha sources activities. These results suggest that in PD patients resting in quiet wakefulness, abnormalities in cortical neural synchronization at alpha frequencies are differently related to cognitive, motor, and visual hallucinations. Interestingly, parallel PD neuropathological processes may have opposite effects on cortical neural synchronization mechanisms generating cortical alpha rhythms in quiet wakefulness.
Abnormalities of cortical neural synchronization mechanisms in patients with dementia due to Alzheimer's and Lewy body diseases: An EEG study
(Elsevier Science Inc., 2017) Babiloni, Claudio; Del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Cordone, Susanna; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Nobili, Flavio; Arnaldi, Dario; Aarsland, Dag; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Onofrj, Marco; Stocchi, Fabrizio; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Caravias, Georg; Garn, Heinrich; Sorpresi, Fabiola; Pievani, Michela; Frisoni, Giovanni B.; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Başar, Erol; Yener, Görsev; Emek-Savaş, Derya Durusu; Triggiani, Antonio Ivano; Franciotti, Raffaella; De Pandis, Maria Francesca; Bonanni, Laura
The aim of this retrospective exploratory study was that resting state eyes-closed electroencephalographic (rsEEG) rhythms might reflect brain arousal in patients with dementia due to Alzheimer's disease dementia (ADD), Parkinson's disease dementia (PDD), and dementia with Lewy body (DLB). Clinical and rsEEG data of 42 ADD, 42 PDD, 34 DLB, and 40 healthy elderly (Nold) subjects were available in an international archive. Demography, education, and Mini-Mental State Evaluation score were not different between the patient groups. Individual alpha frequency peak (IAF) determined the delta, theta, alpha 1, alpha 2, and alpha 3 frequency bands. Fixed beta 1, beta 2, and gamma bands were also considered. rsEEG cortical sources were estimated by means of the exact low-resolution brain electromagnetic source tomography and were then classified across individuals, on the basis of the receiver operating characteristic curves. Compared to Nold, IAF showed marked slowing in PDD and DLB and moderate slowing in ADD. Furthermore, all patient groups showed lower posterior alpha 2 source activities. This effect was dramatic in ADD, marked in DLB, and moderate in PDD. These groups also showed higher occipital delta source activities, but this effect was dramatic in PDD, marked in DLB, and moderate in ADD. The posterior delta and alpha sources allowed good classification accuracy (approximately 0.85-0.90) between the Nold subjects and patients, and between ADD and PDD patients. In quiet wakefulness, delta and alpha sources unveiled different spatial and frequency features of the cortical neural synchronization underpinning brain arousal in ADD, PDD, and DLB patients. Future prospective cross-validation studies should test these rsEEG markers for clinical applications and drug discovery.
Abnormalities of cortical neural synchronization mechanisms in subjects with mild cognitive impairment due to Alzheimer's and Parkinson's diseases: An EEG study
(IOS Press, 2017) Babiloni, Claudio; Del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Cordone, Susanna; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Aarsland, Dag; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Onofrj, Marco; Stocchi, Fabrizio; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Caravias, Georg; Garn, Heinrich; Sorpresi, Fabiola; Pievani, Michela; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Basar, Erol; Yeners, Gorsev; Emek-Savaş, Derya Durusu; Triggiani, Antonio Ivano; Franciotti, Raffaella; Frisoni, Giovanni B.; Bonanni, Laura; De Pandis, Maria Francesca
The aim of this retrospective and exploratory study was that the cortical sources of resting state eyes-closed electroencephalographic (rsEEG) rhythms might reveal different abnormalities in cortical neural synchronization in groups of patients with mild cognitive impairment due to Alzheimer's disease (ADMCI) and Parkinson's disease (PDMCI) as compared to healthy subjects. Clinical and rsEEG data of 75 ADMCI, 75 PDMCI, and 75 cognitively normal elderly (Nold) subjects were available in an international archive. Age, gender, and education were carefully matched in the three groups. The Mini-Mental State Evaluation (MMSE) was matched between the ADMCI and PDMCI groups. Individual alpha frequency peak (IAF) was used to determine the delta, theta, alpha1, alpha2, and alpha3 frequency band ranges. Fixed beta1, beta2, and gamma bands were also considered. eLORETA estimated the rsEEG cortical sources. Receiver operating characteristic curve (ROC) classified these sources across individuals. Results showed that compared to the Nold group, the posterior alpha2 and alpha3 source activities were more abnormal in the ADMCI than the PDMCI group, while the parietal delta source activities were more abnormal in the PDMCI than the ADMCI group. The parietal delta and alpha sources correlated with MMSE score and correctly classified the Nold and diseased individuals (area under the ROC=0.77-0.79). In conclusion, the PDMCI and ADMCI patients showed different features of cortical neural synchronization at delta and alpha frequencies underpinning brain arousal and vigilance in the quiet wakefulness. Future prospective cross-validation studies will have to test these rsEEG markers for clinical applications and drug discovery.
Abnormalities of functional cortical source connectivity of resting-state electroencephalographic alpha rhythms are similar in patients with mild cognitive impairment due to Alzheimer's and Lewy body diseases
(Elsevier Science Inc, 2019) Babiloni, Claudio; del Percio, Claudio; Pascarelli, Maria Teresa; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Rizzo, Marco; Ferri, Rafaele; Soricelli, Andrea; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Salvetti, Marco; Cipollini, Virginia; Franciotti, Raffaella; Onofrj, Marco; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Aarsland, Dag; Parnetti, Lucilla; Farotti, Lucia; Marizzoni, Moira; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Yener, Görsev; Emek Savaş, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; McKeith, Ian; Stocchi, Fabrizio; Vacca, Laura; Hampel, Harald; Frisoni, Giovanni B.; de Pandis, Maria Francesca; Bonanni, Laura
Previous evidence has shown different resting-state eyes-closed electroencephalographic delta (<4 Hz) and alpha (8-10.5 Hz) source connectivity in subjects with dementia due to Alzheimer's (ADD) and Lewy body (DLB) diseases. The present study tested if the same differences may be observed in the prodromal stages of mild cognitive impairment (MCI). Here, clinical and resting-state eyes-closed electroencephalographic data in age-, gender-, and education-matched 30 ADMCI, 23 DLBMCI, and 30 healthy elderly (Nold) subjects were available in our international archive. Mini-Mental State Evaluation (MMSE) score was matched in the ADMCI and DLBMCI groups. The eLORETA freeware estimated delta and alpha source connectivity by the tool called lagged linear connectivity (LLC). Area under receiver operating characteristic curve (AUROCC) indexed the classification accuracy among individuals. Results showed that widespread interhemispheric and intrahemispheric LLC solutions in alpha sources were abnormally lower in both MCI groups compared with the Nold group, but with no differences were found between the 2 MCI groups. AUROCCs of LLC solutions in alpha sources exhibited significant accuracies (0.72-0.75) in the discrimination of Nold versus ADMCI-DLBMCI individuals, but not between the 2 MCI groups. These findings disclose similar abnormalities in ADMCI and DLBMCI patients as revealed by alpha source connectivity. It can be speculated that source connectivity mostly reflects common cholinergic impairment in prodromal state of both AD and DLB, before a substantial dopaminergic derangement in the dementia stage of DLB.
Abnormalities of resting state cortical EEG rhythms in subjects with mild cognitive impairment due to alzheimer's and lewy body diseases
(IOS Press, 2018) Babiloni, Claudio; del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Catania, Valentina; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Aarsland, Dag; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Onofrj, Marco; Stocchi, Fabrizio; Vacca, Laura; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Garn, Heinrich; Fraioli, Lucia; Pievani, Michela; Frisoni, Giovanni B.; D'Antonio, Fabrizia; de Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Başar, Erol; Yener, Görsev; Emek-Savaş, Derya Durusu; Triggiani, Antonio Ivano; Franciotti, Raffaella; Taylor, John Paul; de Pandis, Maria Francesca; Bonanni, Laura
The present study tested the hypothesis that cortical sources of resting state eyes-closed electroencephalographic (rsEEG) rhythms reveal different abnormalities in cortical neural synchronization in groups of patients with mild cognitive impairment due to Alzheimer's disease (ADMCI) and dementia with Lewy bodies (DLBMCI) as compared to cognitively normal elderly (Nold) subjects. Clinical and rsEEG data in 30 ADMCI, 23 DLBMCI, and 30 Nold subjects were available in an international archive. Age, gender, and education were carefully matched in the three groups. The Mini-Mental State Evaluation (MMSE) score was matched between the ADMCI and DLBMCI groups. Individual alpha frequency peak (IAF) was used to determine the delta, theta, alpha1, alpha2, and alpha3 frequency band ranges. Fixed beta1, beta2, and gamma bands were also considered. eLORETA estimated the rsEEG cortical sources. Receiver operating characteristic curve (ROCC) classified these sources across individuals. Compared to Nold, IAF showed marked slowing in DLBMCI and moderate in ADMCI. Furthermore, the posterior alpha 2 and alpha 3 source activities were more abnormal in the ADMCI than the DLBMCI group, while widespread delta source activities were more abnormal in the DLBMCI than the ADMCI group. The posterior delta and alpha sources correlated with the MMSE score and correctly classified the Nold and MCI individuals (area under the ROCC > 0.85). In conclusion, the ADMCI and DLBMCI patients showed different features of cortical neural synchronization at delta and alpha frequencies underpinning brain arousal and vigilance in the quiet wakefulness. Future prospective cross-validation studies will have to test the clinical validity of these rsEEG markers.
Abnormalities of resting-state EEG in patients with prodromal and overt dementia with Lewy bodies: Relation to clinical symptoms
(Elsevier Ireland Ltd, 2020) Pascarelli, Maria Teresa; Del Percio, Claudio; De Pandis, Maria Francesca; Ferri, Raffaele; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Rizzo, Marco; Soricelli, Andrea; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Salvetti, Marco; Cipollini, Virginia; Franciotti, Raffaella; Onofri, Marco; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Aarsland, Dag; Parnetti, Lucilla; Farotti, Lucia; Marizzoni, Moira; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Yener, Görsev; Emek Savaş, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; McKeith, Ian; Stocchi, Fabrizio; Vacca, Laura; Hampel, Harald; Frisoni, Giovanni B.; Bonanni, Laura; Babiloni, Claudio
Objective: Here we tested if cortical sources of resting state electroencephalographic (rsEEG) rhythms may differ in sub-groups of patients with prodromal and overt dementia with Lewy bodies (DLB) as a function of relevant clinical symptoms.Methods: We extracted clinical, demographic and rsEEG datasets in matched DLB patients (N = 60) and control Alzheimer's disease (AD, N = 60) and healthy elderly (Nold, N = 60) seniors from our international database. The eLORETA freeware was used to estimate cortical rsEEG sources.Results: As compared to the Nold group, the DLB and AD groups generally exhibited greater spatially distributed delta source activities (DLB > AD) and lower alpha source activities posteriorly (AD > DLB). As compared to the DLB ``controls", the DLB patients with (1) rapid eye movement (REM) sleep behavior disorders showed lower central alpha source activities (p < 0.005); (2) greater cognitive deficits exhibited higher parietal and central theta source activities as well as higher central, parietal, and occipital alpha source activities (p < 0.01); (3) visual hallucinations pointed to greater parietal delta source activities (p < 0.005).Conclusions: Relevant clinical features were associated with abnormalities in spatial and frequency features of rsEEG source activities in DLB patients.Significance: Those features may be used as neurophysiological surrogate endpoints of clinical symptoms in DLB patients in future cross-validation prospective studies.
Abnormalities of resting-state functional cortical connectivity in patients with dementia due to alzheimer's and lewy body diseases: An EEG study
(Elsevier Science Inc, 2018) Babiloni, Claudio; del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Aarsland, Dag; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Onofrj, Marco; Stocchi, Fabrizio; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Garn, Heinrich; Fraioli, Lucia; Pievani, Michela; Frisoni, Giovanni B.; D'Antonio, Fabrizia; de Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Bazar, Erol; Yener, Görsev; Emek Savaş, Derya Durusu; Triggiani, Antonio Ivano; Franciotti, Raffaella; Taylor, John Paul; Vacca, Laura; de Pandis, Maria Francesca; Bonanni, Laura
Previous evidence showed abnormal posterior sources of resting-state delta (<4 Hz) and alpha (8-12 Hz) rhythms in patients with Alzheimer's disease with dementia (ADD), Parkinson's disease with dementia (PDD), and Lewy body dementia (DLB), as cortical neural synchronization markers in quiet wakefulness. Here, we tested the hypothesis of additional abnormalities in functional cortical connectivity computed in those sources, in ADD, considered as a "disconnection cortical syndrome", in comparison with PDD and DLB. Resting-state eyes-closed electroencephalographic (rsEEG) rhythms had been collected in 42 ADD, 42 PDD, 34 DLB, and 40 normal healthy older (Hold) participants. Exact low-resolution brain electromagnetic tomography (eLORETA) freeware estimated the functional lagged linear connectivity (LLC) from rsEEG cortical sources in delta, theta, alpha, beta, and gamma bands. The area under receiver operating characteristic (AUROC) curve indexed the classification accuracy between Nold and diseased individuals (only values>0.7 were considered). Interhemispheric and intrahemispheric LLCs in widespread delta sources were abnormally higher in the ADD group and, unexpectedly, normal in DLB and PDD groups. Intrahemispheric LLC was reduced in widespread alpha sources dramatically in ADD, markedly in DLB, and moderately in PDD group. Furthermore, the interhemispheric LLC in widespread alpha sources showed lower values in ADD and DLB than PDD groups. At the individual level, AUROC curves of LLC in alpha sources exhibited better classification accuracies for the discrimination of ADD versus Nold individuals (0.84) than for DLB versus Nold participants (0.78) and PDD versus Nold participants (0.75). Functional cortical connectivity markers in delta and alpha sources suggest a more compromised neurophysiological reserve in ADD than DLB, at both group and individual levels.
Are there consistent abnormalities in event-related EEG oscillations in patients with Alzheimer's disease compared to other diseases belonging to dementia?
(John Wiley and Sons Inc, 2022) Güntekin, Bahar; Aktürk, Tuba; Arakaki, Xianghong; Bonanni, Laura; Del Percio, Claudio; Edelmayer, Rebecca; Farina, Francesca; Ferri, Raffaele; Hanoğlu, Lütfü; Kumar, Sanjeev; Lizio, Roberta; Lopez, Susanna; Murphy, Brian; Noce, Giuseppe; Randall, Fiona; Sack, Alexander T.; Stocchi, Fabrizio; Yener, Görsev; Yıldırım, Ebru; Babiloni, Claudio
Cerebrospinal and structural-molecular neuroimaging in-vivo biomarkers are recommended for diagnostic purposes in Alzheimer’s disease (AD) and other dementias; however, they do not explain the effects of AD neuropathology on neurophysiological mechanisms underpinning cognitive processes. Here, an Expert Panel from the Electrophysiology Professional Interest Area of the Alzheimer’s Association reviewed the field literature and reached consensus on the event-related electroencephalographic oscillations (EROs) that show consistent abnormalities in patients with significant cognitive deficits due to Alzheimer’s, Parkinson’s (PD), Lewy body (LBD), and cerebrovascular diseases. Converging evidence from oddball paradigms showed that, as compared to cognitively unimpaired (CU) older adults, AD patients had lower amplitude in widespread delta (>4 Hz) and theta (4–7 Hz) phase-locked EROs as a function of disease severity. Similar effects were also observed in PD, LBD, and/or cerebrovascular cognitive impairment patients. Non-phase-locked alpha (8–12 Hz) and beta (13–30 Hz) oscillations were abnormally reduced (event-related desynchronization, ERD) in AD patients relative to CU. However, studies on patients with other dementias remain lacking. Delta and theta phase-locked EROs during oddball tasks may be useful neurophysiological biomarkers of cognitive systems at work in heuristic and intervention clinical trials performed in AD patients, but more research is needed regarding their potential role for other dementias.
Classification of patients with alzheimer's disease and dementia with lewy bodies using resting EEG selected features at sensor and source levels: A proof-of-concept study
(Bentham Science, 2021) San Martin, Rodrigo; J Fraga, Francisco; Del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Nobili, Flavio; Arnaldi, Dario; D'Antonio, Fabrizia; Lena, Carlo De; Güntekin, Bahar; Hanoğlu, Lütfü; Taylor, John Paul; McKeith, Ian; Stocchi, Fabrizio; Ferri, Raffaele; Onofrj, Marco; Lopez, Susanna; Bonanni, Laura; Babiloni, Claudio
Background: Early differentiation between Alzheimer's disease (AD) and Dementia with Lewy Bodies (DLB) is important for accurate prognosis, as DLB patients typically show faster disease progression. Cortical neural networks, necessary for human cognitive function, may be disrupted differently in DLB and AD patients, allowing diagnostic differentiation between AD and DLB. Objective: This proof-of-concept study assessed whether the application of machine learning techniques to data derived from resting-state electroencephalographic (rsEEG) rhythms (discriminant sensor power, 19 electrodes) and source connectivity (between five cortical regions of interest) allowed differentiation between DLB and AD. Methods: Clinical, demographic, and rsEEG datasets from DLB patients (N=30), AD patients (N=30), and control seniors (NOld, N=30), matched for age, sex, and education, were taken from our international database. Individual (delta, theta, alpha) and fixed (beta) rsEEG frequency bands were included. The rsEEG features for the classification task were computed at both sensor and source levels. The source level was based on eLORETA freeware toolboxes for estimating cortical source activity and linear lagged connectivity. Fluctuations of rsEEG recordings (band-pass waveform envelopes of each EEG rhythm) were also computed at both sensor and source levels. After blind feature reduction, rsEEG features served as input to support vector machine (SVM) classifiers. Discrimination of individuals from the three groups was measured with standard performance metrics (accuracy, sensitivity, and specificity). Results: The trained SVM two-class classifiers showed classification accuracies of 97.6% for NOld vs. AD, 99.7% for NOld vs. DLB, and 97.8% for AD vs. DLB. Three-class classifiers (AD vs. DLB vs. NOld) showed classification accuracy of 94.79%. Conclusion: These promising preliminary results should encourage future prospective and longitudinal cross-validation studies using higher resolution EEG techniques and harmonized clinical procedures to enable the clinical application of these machine learning techniques.
Corrigendum to ‘‘Functional cortical source connectivity of resting stateelectroencephalographic alpha rhythms shows similar abnormalitiesin patients with mild cognitive impairment due to Alzheimer’s and Parkinson’s diseases” [Clin. Neurophysiol. 129 (2018) 766–782]
(Elsevier Ireland Ltd., 2019) Babiloni, Claudio; Percio, Claudio Del; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Catania, Valentina; Nobili, Flavio; Arnaldi, Dario; Famà, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Bonanni, Laura; Franciotti, Raffaella; Onofrj, Marco; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Garn, Heinrich; Fraioli, Lucia; Pievani, Michela; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Başar, Erol; Yener, Görsev; Emek-Savaş, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; De Pandis, Maria Francesca; Vacca, Laura; Stocchi, Fabrizio
Objective: This study tested the hypothesis that markers of functional cortical source connectivity of resting state eyes-closed electroencephalographic (rsEEG) rhythms may be abnormal in subjects with mild cognitive impairment due to Alzheimer’s (ADMCI) and Parkinson’s (PDMCI) diseases compared to healthy elderly subjects (Nold). Methods: rsEEG data had been collected in ADMCI, PDMCI, and Nold subjects (N?=?75 for any group). eLORETA freeware estimated functional lagged linear connectivity (LLC) from rsEEG cortical sources. Area under receiver operating characteristic (AUROC) curve indexed the accuracy in the classification of Nold and MCI individuals. Results: Posterior interhemispheric and widespread intrahemispheric alpha LLC solutions were abnormally lower in both MCI groups compared to the Nold group. At the individual level, AUROC curves of LLC solutions in posterior alpha sources exhibited moderate accuracies (0.70–0.72) in the discrimination of Nold vs. ADMCI-PDMCI individuals. No differences in the LLC solutions were found between the two MCI groups. Conclusions: These findings unveil similar abnormalities in functional cortical connectivity estimated in widespread alpha sources in ADMCI and PDMCI. This was true at both group and individual levels. Significance: The similar abnormality of alpha source connectivity in ADMCI and PDMCI subjects might reflect common cholinergic impairment.
EEG measures for clinical research in major vascular cognitive impairment: recommendations by an expert panel
(Elsevier Inc., 2021) Babiloni, Claudio C.; Arakaki, Xianghong; Bonanni, Laura; Buján, Ana; Carrillo, María C.; del Percio, Claudio; Edelmayer, Rebecca M.; Egan, Gary; Elahh, Fanny M.; Evans, Alan Charles; Ferri, Raffaele; Frisoni, Glovannl B.; Güntekin, Bahar; Hainsworth, Atticus Henry; Hampel, Harald; Jeli?, Vesna; Jeong, Jaeseung; Kim, Doh-kwan; Kramberger, Milica Gregori?; Kumar, Sanjeev; Lizio, Roberta; Nobili, Flavio Mariano; Noce, Giuseppe; Puce, Aina; Ritter, Petra; Smit, Dirk J.A.; Soricelli, Andrea; Teipel, S.; Tucci, Federico
Vascular contribution to cognitive impairment (VCI) and dementia is related to etiologies that may affect the neurophysiological mechanisms regulating brain arousal and generating electroencephalographic (EEG) activity. A multidisciplinary expert panel reviewed the clinical literature and reached consensus about the EEG measures consistently found as abnormal in VCI patients with dementia. As compared to cognitively unimpaired individuals, those VCI patients showed (1) smaller amplitude of resting state alpha (8–12 Hz) rhythms dominant in posterior regions; (2) widespread increases in amplitude of delta (< 4 Hz) and theta (4–8 Hz) rhythms; and (3) delayed N200/P300 peak latencies in averaged event-related potentials, especially during the detection of auditory rare target stimuli requiring participants’ responses in “oddball” paradigms. The expert panel formulated the following recommendations: (1) the above EEG measures are not specific for VCI and should not be used for its diagnosis; (2) they may be considered as “neural synchronization” biomarkers to enlighten the relationships between features of the VCI-related cerebrovascular lesions and abnormalities in neurophysiological brain mechanisms; and (3) they may be tested in future clinical trials as prognostic biomarkers and endpoints of interventions aimed at normalizing background brain excitability and vigilance in wakefulness.
Functional cortical source connectivity of resting state electroencephalographic alpha rhythms shows similar abnormalities in patients with mild cognitive impairment due to Alzheimer's and Parkinson's diseases
(Elsevier Ireland Ltd, 2018) Babiloni, Claudio; Del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Catania, Valentina; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Bonanni, Laura; Franciotti, Raffaella; Onofrj, Marco; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Garn, Heinrich; Fraioli, Lucia; Pievanim, Michela; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Başar, Erol; Yener, Görsev; Emek-Savas, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; De Pandis, Maria Francesca; Vacca, Laura; Frisoni, Giovanni B.; Stocchi, Fabrizio
Objective: This study tested the hypothesis that markers of functional cortical source connectivity of resting state eyes-closed electroencephalographic (rsEEG) rhythms may be abnormal in subjects with mild cognitive impairment due to Alzheimer's (ADMCI) and Parkinson's (PDMCI) diseases compared to healthy elderly subjects (Nold). Methods: rsEEG data had been collected in ADMCI, PDMCI, and Nold subjects (N = 75 for any group). eLORETA freeware estimated functional lagged linear connectivity (LLC) from rsEEG cortical sources. Area under receiver operating characteristic (AUROC) curve indexed the accuracy in the classification of Nold and MCI individuals. Results: Posterior interhemispheric and widespread intrahemispheric alpha LLC solutions were abnormally lower in both MCI groups compared to the Nold group. At the individual level, AUROC curves of LLC solutions in posterior alpha sources exhibited moderate accuracies (0.70-0.72) in the discrimination of Nold vs. ADMCI-PDMCI individuals. No differences in the LLC solutions were found between the two MCI groups. Conclusions: These findings unveil similar abnormalities in functional cortical connectivity estimated in widespread alpha sources in ADMCI and PDMCI. This was true at both group and individual levels. Significance: The similar abnormality of alpha source connectivity in ADMCI and PDMCI subjects might reflect common cholinergic impairment.
Levodopa may affect cortical excitability in Parkinson's disease patients with cognitive deficits as revealed by reduced activity of cortical sources of resting state electroencephalographic rhythms
(Elsevier Science Inc, 2019) Babiloni, Claudio; del Percio, Claudio; Lizio, Roberta; Noce, Giuseppe; Lopez, Susanna; Soricelli, Andrea; Ferri, Raffaele; Pascarelli, Maria Teresa; Catania, Valentine; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Orzi, Francesco; Buttinelli, Carla; Giubilei, Franco; Bonanni, Laura; Franciotti, Raffaella; Onofrj, Marco; Stirpe, Paola; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Fraioli, Lucia; Parnetti, Lucilla; Farotti, Lucia; Pievani, Michela; D'Antonio, Fabrizia; de Lena, Carlo; Güntekin, Bahar; Hanoğlu, Lütfü; Yener, Görsev; Emek Savaş, Derya Durusu; Triggiani, Antonio Ivano; Taylor, John Paul; McKeith, Ian; Stocchi, Fabrizio; Vacca, Laura; Frisoni, Giovanni B.; de Pandis, Maria Francesca
We hypothesized that dopamine neuromodulation might affect cortical excitability in Parkinson's disease (PD) patients set in quiet wakefulness, as revealed by resting state eyes-closed electroencephalographic (rsEEG) rhythms at alpha frequencies (8-12 Hz). Clinical and rsEEG rhythms in PD with dementia (N = 35), PD with mild cognitive impairment (N = 50), PD with normal cognition (N = 35), and normal (N = 50) older adults were available from an international archive. Cortical rsEEG sources were estimated by exact low-resolution brain electromagnetic tomography. Compared with the normal older group, the PD groups showed reduced occipital alpha sources and increased widespread delta (<4 Hz) sources. Widespread frontal and temporal alpha sources exhibited an increase in PD with dementia compared with PD with mild cognitive impairment and PD with normal cognition groups, as function of dopamine depletion severity, typically greater in the former than the latter groups. A daily dose of levodopa induced a widespread reduction in cortical delta and alpha sources in a subgroup of 13 PD patients under standard chronic dopaminergic regimen. In PD patients in quiet wakefulness, alpha cortical source activations may reflect an excitatory effect of dopamine neuromodulation.
Measures of resting state EEG rhythms for clinical trials in Alzheimer's disease: Recommendations of an expert panel
(Wiley, 2021) Babiloni, Claudio; Arakaki, Xianghong; Azami, Hamed; Bennys, Karim; Blinowska, Katarzyna; Bonanni, Laura; Bujan, Ana; Carrillo, Maria C.; Cichocki, Andrzej; de Frutos-Lucas, Jaisalmer; del Percio, Claudio; Dubois, Bruno; Edelmayer, Rebecca; Egan, Gary; Epelbaum, Stephane; Escudero, Javier; Evans, Alan; Farina, Francesca; Fargo, Keith; Fernandez, Alberto; Ferri, Raffaele; Frisoni, Giovanni; Hampel, Harald; Harrington, Michael G.; Jelic, Vesna; Jeong, Jaeseung; Jiang, Yang; Kaminski, Maciej; Kavcic, Voyko; Kilborn, Kerry; Kumar, Sanjeev; Lam, Alice; Lim, Lew; Lizio, Roberta; Lopez, David; Lopez, Susanna; Lucey, Brendan; Maestu, Fernando; McGeown, William J.; McKeith, Ian; Moretti, Davide Vito; Nobili, Flavio; Noce, Giuseppe; Olichney, John; Onofrj, Marco; Osorio, Ricardo; Parra-Rodriguez, Mario; Rajji, Tarek; Ritter, Petra; Soricelli, Andrea; Stocchi, Fabrizio; Tarnanas, Ioannis; Taylor, John Paul; Teipel, Stefan; Tucci, Federico; Valdes-Sosa, Mitchell; Valdes-Sosa, Pedro; Weiergraeber, Marco; Yener, Görsev; Güntekin, Bahar
The Electrophysiology Professional Interest Area (EPIA) and Global Brain Consortium endorsed recommendations on candidate electroencephalography (EEG) measures for Alzheimer's disease (AD) clinical trials. The Panel reviewed the field literature. As most consistent findings, AD patients with mild cognitive impairment and dementia showed abnormalities in peak frequency, power, and "interrelatedness" at posterior alpha (8-12 Hz) and widespread delta (< 4 Hz) and theta (4-8 Hz) rhythms in relation to disease progression and interventions. The following consensus statements were subscribed: (1) Standardization of instructions to patients, resting state EEG (rsEEG) recording methods, and selection of artifact-free rsEEG periods are needed; (2) power density and "interrelatedness" rsEEG measures (e.g., directed transfer function, phase lag index, linear lagged connectivity, etc.) at delta, theta, and alpha frequency bands may be use for stratification of AD patients and monitoring of disease progression and intervention; and (3) international multisectoral initiatives are mandatory for regulatory purposes.
Reactivity of posterior cortical electroencephalographic alpha rhythms during eyes opening in cognitively intact older adults and patients with dementia due to Alzheimer's and Lewy body diseases
(Elsevier Inc., 2022) Babiloni, Claudio; Lorenzo, Ivan; Lizio, Roberta; Lopez, Susanna; Tucci, Federico; Ferri, Raffaele; Soricelli, Andrea; Nobili, Flavio; Arnaldi, Dario; Famà, Francesco; Buttinelli, Carla; Giubilei, Franco; Cipollini, Virginia; Onofrj, Marco; Stocchi, Fabrizio; Vacca, Laura; Fuhr, Peter; Gschwandtner, Ute; Ransmayr, Gerhard; Aarsland, Dag; Parnetti, Lucilla; Marizzoni, Moira; D'Antonio, Fabrizia; De Lena, Carlo; Güntekin, Bahar; Yıldırım, Ebru; Hanoğlu, Lütfü; Yener, Görsev; Hünerli Gündüz, Duygu; Taylor, John Paul; Schumacher, Julia; McKeith, Ian; Frisoni, Giovanni B.; De Pandis, Maria Francesca; Bonanni, Laura; Percio, Claudio Del; Noce, Giuseppe
Please modify the Abstract as follows:Here we tested if the reactivity of posterior resting-state electroencephalographic (rsEEG) alpha rhythms from the eye-closed to the eyes-open condition may differ in patients with dementia due to Lewy Bodies (DLB) and Alzheimer's disease (ADD) as a functional probe of the dominant neural synchronization mechanisms regulating the vigilance in posterior visual systems.We used clinical, demographical, and rsEEG datasets in 28 older adults (Healthy), 42 DLB, and 48 ADD participants. The eLORETA freeware was used to estimate cortical rsEEG sources.Results showed a substantial (> -10%) reduction in the posterior alpha activities during the eyes-open condition in 24 Healthy, 26 ADD, and 22 DLB subjects. There were lower reductions in the posterior alpha activities in the ADD and DLB groups than in the Healthy group. That reduction in the occipital region was lower in the DLB than in the ADD group.These results suggest that DLB patients may suffer from a greater alteration in the neural synchronization mechanisms regulating vigilance in occipital cortical systems compared to ADD patients.
Relationship between default mode network and resting-state electroencephalographic alpha rhythms in cognitively unimpaired seniors and patients with dementia due to Alzheimer's disease
(Oxford University Press Inc., 2023) Babiloni, Claudio; Lopez, Susanna; Noce, Giuseppe; Ferri, Raffaele; Panerai, Simonetta; Catania, Valentina; Soricelli, Andrea; Salvatore, Marco; Nobili, Flavio; Arnaldi, Dario; Fama, Francesco; Massa, Federico; Buttinelli, Carla; Giubilei, Franco; Stocchi, Fabrizio; Vacca, Laura; Marizzoni, Moira; D'Antonio, Fabrizia; Bruno, Giuseppe; de Lena, Carlo; Güntekin, Bahar; Yıldırım, Ebru; Hanoğlu, Lütfü; Yener, Görsev; Yerlikaya, Deniz; Taylor, John Paul; Schumacher, Julia; Mckeith, Ian; Bonanni, Laura; Pantano, Patrizia; Piervincenzi, Claudia; Petsas, Nikolaos; Frisoni, Giovanni B.; del Percio, Claudio; Carducci, Filippo
Here we tested the hypothesis of a relationship between the cortical default mode network (DMN) structural integrity and the resting state electroencephalographic (rsEEG) rhythms in patients with Alzheimer's disease with dementia (ADD). Clinical and instrumental datasets in 45 ADD patients and 40 normal elderly (Nold) persons originated from the PDWAVES Consortium (www.pdwaves.eu). Individual rsEEG delta, theta, alpha, and fixed beta and gamma bands were considered. Freeware platforms served to derive (1) the (gray matter) volume of the DMN, dorsal attention (DAN), and sensorimotor (SMN) cortical networks and (2) the rsEEG cortical eLORETA source activities. We found a significant positive association between the DMN gray matter volume, the rsEEG alpha source activity estimated in the posterior DMN nodes (parietal and posterior cingulate cortex), and the global cognitive status in the Nold and ADD participants. Compared with the Nold, the ADD group showed lower DMN gray matter, lower rsEEG alpha source activity in those nodes, and lower global cognitive status. This effect was not observed in the DAN and SMN. These results suggest that the DMN structural integrity and the rsEEG alpha source activities in the DMN posterior hubs may be related and predict the global cognitive status in ADD and Nold persons.
Treatment effects on event-related EEG potentials and oscillations in Alzheimer's disease
(Elsevier B.V., 2022) Yener, Görsev; Hünerli Gündüz, Duygu; Yıldırım, Ebru; Aktürk, Tuba; Başar Eroğlu, Canan; Bonanni, Laura; Del Percio, Claudio; Farina, Francesca; Ferri, Raffaele; Güntekin, Bahar; Hajós, Mihály; Ibáñez, Agustín; Jiang, Yang; Lizio, Roberta; Lopez, Susanna; Noce, Giuseppe; Parra, Mario A.; Randall, Fiona; Stocchi, Fabrizio; Babiloni, Claudio
Alzheimer's disease dementia (ADD) is the most diffuse neurodegenerative disorder belonging to mild cognitive impairment (MCI) and dementia in old persons. This disease is provoked by an abnormal accumulation of amyloid-beta and tauopathy proteins in the brain. Very recently, the first disease-modifying drug has been licensed with reserve (i.e., Aducanumab). Therefore, there is a need to identify and use biomarkers probing the neurophysiological underpinnings of human cognitive functions to test the clinical efficacy of that drug. In this regard, event-related electroencephalographic potentials (ERPs) and oscillations (EROs) are promising candidates. Here, an Expert Panel from the Electrophysiology Professional Interest Area of the Alzheimer's Association and Global Brain Consortium reviewed the field literature on the effects of the most used symptomatic drug against ADD (i.e., Acetylcholinesterase inhibitors) on ERPs and EROs in ADD patients with MCI and dementia at the group level. The most convincing results were found in ADD patients. In those patients, Acetylcholinesterase inhibitors partially normalized ERP P300 peak latency and amplitude in oddball paradigms using visual stimuli. In these same paradigms, those drugs partially normalize ERO phase-locking at the theta band (4–7 Hz) and spectral coherence between electrode pairs at the gamma (around 40 Hz) band. These results are of great interest and may motivate multicentric, double-blind, randomized, and placebo-controlled clinical trials in MCI and ADD patients for final cross-validation.
What electrophysiology tells us about Alzheimer's disease: A window into the synchronization and connectivity of brain neurons
(Elsevier, 2020) Babiloni, Claudio; Blinowska, Katarzyna Joanna; Bonanni, Laura; Cichocki, Andrzej; De Haan, Willem; Del Percio, Claudio; Dubois, Bruno; Escudero, Javier; Fernández, Alberto; Frisoni, Giovanni Battista; Güntekin, Bahar; Hajo?, Mihály; Hampel, Harald; Ifeachor, Emmanuel C.; Kilborn, Kerry W.; Kumar, Sanjeev; Johnsen, Kristinn; Johannsson, Magnus; Jeong, Jaeseung; Lebeau, Fiona E.N.; Lizio, Roberta; Lopes da Silva, Fernando H.; Maestu, Fernando; McGeown, William Jonathan; Mckeith, Ian G.; Moretti, Davide Vito; Nobili, Flavio Mariano; Olichney, John; Onofrj, Marco; Palop, Jorge J.; Rowan, Michael; Stocchi, Fabrizio; Struzik, Zbigniew Romuald; Tanila, Heikki; Teipel, Stephan; Taylor, John-Paul; Weiergräber, Marco; Yener, Görsev; Young-Pearse, Tracy; Drinkenburg, Wilhelmus H.; Randall, Fiona
Electrophysiology provides a real-time readout of neural functions and network capability in different brain states, on temporal (fractions of milliseconds) and spatial (micro, meso, and macro) scales unmet by other methodologies. However, current international guidelines do not endorse the use of electroencephalographic (EEG)/magnetoencephalographic (MEG) biomarkers in clinical trials performed in patients with Alzheimer's disease (AD), despite a surge in recent validated evidence. This position paper of the ISTAART Electrophysiology Professional Interest Area endorses consolidated and translational electrophysiological techniques applied to both experimental animal models of AD and patients, to probe the effects of AD neuropathology (i.e., brain amyloidosis, tauopathy, and neurodegeneration) on neurophysiological mechanisms underpinning neural excitation/inhibition and neurotransmission as well as brain network dynamics, synchronization, and functional connectivity, reflecting thalamocortical and corticocortical residual capacity. Converging evidence shows relationships between abnormalities in EEG/MEG markers and cognitive deficits in groups of AD patients at different disease stages. The supporting evidence for the application of electrophysiology in AD clinical research as well as drug discovery pathways warrants an international initiative to include the use of EEG/MEG biomarkers in the main multicentric projects planned in AD patients, to produce conclusive findings challenging the present regulatory requirements and guidelines for AD studies.

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