[en] The characterization of the distinct dynamic functional connectivity (dFC) patterns that activate in the brain during rest can help to understand the underlying time-varying network organization. The presence and behavior of these patterns (known as meta-states) have been widely studied by means of functional magnetic resonance imaging (fMRI). However, modalities with high-temporal resolution, such as electroencephalography (EEG), enable the characterization of fast temporally evolving meta-state sequences. Mild cognitive impairment (MCI) and dementia due to Alzheimer's disease (AD) have been shown to disrupt spatially localized activation and dFC between different brain regions, but not much is known about how they affect meta-state network topologies and their network dynamics. The main hypothesis of the study was that MCI and dementia due to AD alter normal meta-state sequences by inducing a loss of structure in their patterns and a reduction of their dynamics. Moreover, we expected that patients with MCI would display more flexible behavior compared to patients with dementia due to AD. Thus, the aim of the current study was twofold: (i) to find repeating, distinctly organized network patterns (meta-states) in neural activity; and (ii) to extract information about meta-state fluctuations and how they are influenced by MCI and dementia due to AD. To accomplish these goals, we present a novel methodology to characterize dynamic meta-states and their temporal fluctuations by capturing aspects based on both their discrete activation and the continuous evolution of their individual strength. These properties were extracted from 60-s resting-state EEG recordings from 67 patients with MCI due to AD, 50 patients with dementia due to AD, and 43 cognitively healthy controls. First, the instantaneous amplitude correlation (IAC) was used to estimate instantaneous functional connectivity with a high temporal resolution. We then extracted meta-states by means of graph community detection based on recurrence plots (RPs), both at the individual- and group-level. Subsequently, a diverse set of properties of the continuous and discrete fluctuation patterns of the meta-states was extracted and analyzed. The main novelty of the methodology lies in the usage of Louvain GJA community detection to extract meta-states from IAC-derived RPs and the extended analysis of their discrete and continuous activation. Our findings showed that distinct dynamic functional connectivity meta-states can be found on the EEG time-scale, and that these were not affected by the oscillatory slowing induced by MCI or dementia due to AD. However, both conditions displayed a loss of meta-state modularity, coupled with shorter dwell times and higher complexity of the meta-state sequences. Furthermore, we found evidence that meta-state sequencing is not entirely random; it shows an underlying structure that is partially lost in MCI and dementia due to AD. These results show evidence that AD progression is associated with alterations in meta-state switching, and a degradation of dynamic brain flexibility.
Disciplines :
Neurology
Author, co-author :
Nunez Novo, Pablo ; University of Valladolid > Biomedical Engineering Group
Poza, Jesús ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain, Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Madrid, Spain, IMUVA, Instituto de Investigación en Matemáticas, University of Valladolid, Spain
Gómez, Carlos ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain, Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Madrid, Spain
Rodríguez-González, Víctor ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain
Hillebrand, Arjan ; Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam, The Netherlands
Tewarie, Prejaas; Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, Amsterdam, The Netherlands
Tola-Arribas, Miguel Ángel; Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Madrid, Spain
Cano, Mónica; Department of Clinical Neurophysiology, "Río Hortega" University Hospital, Valladolid, Spain
Hornero, Roberto ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain, Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Madrid, Spain, IMUVA, Instituto de Investigación en Matemáticas, University of Valladolid, Spain
Language :
English
Title :
Abnormal meta-state activation of dynamic brain networks across the Alzheimer spectrum.
EC - European Commission ERDF - European Regional Development Fund
Funding text :
This research was supported by ‘Ministerio de Ciencia e Innovación - Agencia Estatal de Investigación’ and ‘European Regional Development Fund’ (FEDER) and ‘Ministerio de Ciencia, Innovación y Universidades’ under projects PGC2018-098214-A-I00, the ‘European Commission’ and FEDER under project ‘Análisis y correlación entre el genoma completo y la actividad cerebral para la ayuda en el diagnóstico de la enfermedad de Alzheimer’ and ‘Análisis y correlación entre la epigenética y la actividad cerebral para evaluar el riesgo de migraña crónica y episódica en mujeres’ (‘Cooperation Programme Interreg V-A Spain-Portugal POCTEP 2014–2020’), and by CIBER-BBN (ISCIII) co-funded with FEDER funds. P. Núñez was in receipt of a predoctoral scholarship ‘Ayuda para contratos predoctorales para la Formación de Profesorado Universitario (FPU)’ grant from the ‘Ministerio de Educación, Cultura y Deporte’ (FPU17/00850). V. Rodríguez-González was in receipt of a PIF-UVa grant from the ‘University of Valladolid’.This research was supported by ?Ministerio de Ciencia e Innovaci?n - Agencia Estatal de Investigaci?n? and ?European Regional Development Fund? (FEDER) and ?Ministerio de Ciencia, Innovaci?n y Universidades? under projects PGC2018-098214-A-I00, the ?European Commission? and FEDER under project ?An?lisis y correlaci?n entre el genoma completo y la actividad cerebral para la ayuda en el diagn?stico de la enfermedad de Alzheimer? and ?An?lisis y correlaci?n entre la epigen?tica y la actividad cerebral para evaluar el riesgo de migra?a cr?nica y epis?dica en mujeres? (?Cooperation Programme Interreg V-A Spain-Portugal POCTEP 2014?2020?), and by CIBER-BBN (ISCIII) co-funded with FEDER funds. P. N??ez was in receipt of a predoctoral scholarship ?Ayuda para contratos predoctorales para la Formaci?n de Profesorado Universitario (FPU)? grant from the ?Ministerio de Educaci?n, Cultura y Deporte? (FPU17/00850). V. Rodr?guez-Gonz?lez was in receipt of a PIF-UVa grant from the ?University of Valladolid?.
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