Connectivity strength of the EEG functional network in schizophrenia and bipolar disorder.

Bipolar disorder; Connectivity strength; Functional network; Graph-theory; Schizophrenia; Antipsychotic Agents; Adult; Antipsychotic Agents/therapeutic use; Bipolar Disorder/physiopathology; Bipolar Disorder/psychology; Cognition; Event-Related Potentials, P300; Female; Humans; Male; Middle Aged; Nerve Net/physiopathology; Neural Pathways/physiopathology; Schizophrenia/physiopathology; Schizophrenic Psychology; Theta Rhythm; Treatment Outcome; Young Adult; Electroencephalography; Nerve Net; Neural Pathways; Pharmacology; Biological Psychiatry

Abstract :

[en] The application of graph theory measures in the study of functional brain networks allows for the description of their general properties and their alterations in mental illness. Among these measures, connectivity strength (CS) estimates the degree of functional connectivity of the whole network. Previous studies in schizophrenia patients have reported higher baseline CS values and modulation deficits in EEG spectral properties during cognitive activity. The specificity of these alterations and their relationships with pharmacological treatments remain unknown. Therefore, in the present study, we assessed functional CS on EEG-based brain networks in 79 schizophrenia and 29 bipolar patients in addition to 63 healthy controls. The subjects performed a P300 task during the EEG recordings from which the pre-stimulus and the task-related modulation CS values were computed in the global and theta bands. These values were compared between the groups and between the patients who had and had not received different treatments. The global band pre-stimulus CS was significantly higher in the schizophrenia group compared with the bipolar and control groups. Theta band CS modulation was decreased in schizophrenia and bipolar patients. Treatment with antipsychotics, lithium, benzodiazepines, and anticonvulsants did not significantly alter these CS values. The first-episode and chronic schizophrenia patients did not show significant differences in CS values. Higher global band pre-stimulus CS values were associated with worse general cognition in schizophrenia patients. These data support increased connectivity in the whole-brain network that is specific to schizophrenia and suggest a general hyper-synchronized basal state that might hamper cognition in this syndrome.

Disciplines :

Psychiatry

Author, co-author :

Cea-Cañas, Benjamín; Clinical Neurophysiology Service, Clinical Hospital of Valladolid, Ramón y Cajal, 3, 47003 Valladolid, Spain

Gomez-Pilar, Javier; Biomedical Engineering Group, University of Valladolid, Paseo de Belén, 15, 47011 Valladolid, Spain

Nunez Novo, Pablo ; University of Valladolid > Biomedical Engineering Group

Rodríguez-Vázquez, Eva; Psychiatry Service, Clinical Hospital of Valladolid, Ramón y Cajal, 3, 47003 Valladolid, Spain

de Uribe, Nieves; Psychiatry Service, Clinical Hospital of Valladolid, Ramón y Cajal, 3, 47003 Valladolid, Spain

Díez, Álvaro; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005 Valladolid, Spain

Pérez-Escudero, Adela; Psychiatry Service, Clinical Hospital of Valladolid, Ramón y Cajal, 3, 47003 Valladolid, Spain

Molina, Vicente; Psychiatry Service, Clinical Hospital of Valladolid, Ramón y Cajal, 3, 47003 Valladolid, Spain, Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005 Valladolid, Spain, Neurosciences Institute of Castilla y León (INCYL), School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005 Valladolid, Spain. Electronic address: vicente.molina@uva.es

Language :

English

Title :

Connectivity strength of the EEG functional network in schizophrenia and bipolar disorder.

Publication date :

02 March 2020

Journal title :

Progress in Neuro-Psychopharmacology and Biological Psychiatry

ISSN :

0278-5846

eISSN :

1878-4216

Publisher :

Elsevier Inc., England

Volume :

Pages :

109801

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0278584619304725?httpAccept=text/xml

Funders :

ISCIII - Instituto de Salud Carlos III
JCYL - Junta de Castilla y León

Funding text :

This work has been supported by the following grants: the “ Instituto de Salud Carlos III ” ( PI15/00299 and PI18/00178 ), the “Gerencia Regional de Salud de Castilla y León” ( GRS 1485/A/17 and GRS 1721/A/18 ), and the “ Consejería de Educación de la Junta de Castilla y León ” ( VA059U13 and VA057P17 ). 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 ).

Available on ORBi :

since 17 May 2023

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Bibliography

Bachiller, A., Díez, A., Suazo, V., Domínguez, C., Ayuso, M., Hornero, R., Molina, V., Decreased spectral entropy modulation in patients with schizophrenia during a P300 task. Eur. Arch. Psychiatry Clin. Neurosci. 264:6 (2014), 533–543, 10.1007/s00406-014-0488-6.
Bachiller, A., Poza, J., Gómez, C., Molina, V., Suazo, V., Hornero, R., A comparative study of event-related coupling patterns during an auditory oddball task in schizophrenia. J. Neural Eng., 12(1), 2015, 016007, 10.1088/1741-2560/12/1/016007.
Başar-Eroglu, C., Demiralp, T., Event-related theta oscillations: an integrative and comparative approach in the human and animal brain. Int. Psychophysiol. 39:2–3 (2001), 167–195 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11163896.
Bastos, A.M., Schoffelen, J.-M., A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Frontiers in Systems Neuroscience, 2016 Retrieved from https://www.frontiersin.org/article/10.3389/fnsys.2015.00175.
Bledowski, C., Prvulovic, D., Hoechstetter, K., Scherg, M., Wibral, M., Goebel, R., Linden, D.E.J., Localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. J. Neurosci. 24:42 (2004), 9353–9360, 10.1523/JNEUROSCI.1897-04.2004.
Bob, P., Palus, M., Susta, M., Glaslova, K., EEG phase synchronization in patients with paranoid schizophrenia. Neurosci. Lett. 447:1 (2008), 73–77, 10.1016/j.neulet.2008.09.055.
Buzsáki, G., Rhythms of the Brain. 2006, Oxford University Press Retrieved from https://global.oup.com/academic/product/rhythms-of-the-brain-9780199828234?cc=es&lang=en&.
Buzsaki, G., Draguhn, A., Neuronal oscillations in cortical networks. Science 304:5679 (2004), 1926–1929, 10.1126/science.1099745.
Cea-Cañas, B., de Luis, R., Lubeiro, A., Gomez-Pilar, J., Sotelo, E., del Valle, P., Molina, V., Structural connectivity in schizophrenia and bipolar disorder: effects of chronicity and antipsychotic treatment. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 92 (2019), 369–377, 10.1016/j.pnpbp.2019.02.006.
Devrim, M., Demiralp, T., Ademoglu, A., Kurt, A., A model for P300 generation based on responses to near-threshold visual stimuli. Brain Res. Cogn. Brain Res. 8:1 (1999), 37–43 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10216272.
Fee, C., Banasr, M., Sibille, E., Somatostatin-positive gamma-aminobutyric acid interneuron deficits in depression: cortical microcircuit and therapeutic perspectives. Biol. Psychiatry 82:8 (2017), 549–559, 10.1016/j.biopsych.2017.05.024.
Gomez-Pilar, J., Lubeiro, A., Poza, J., Hornero, R., Ayuso, M., Valcárcel, C., Molina, V., Functional EEG network analysis in schizophrenia: evidence of larger segregation and deficit of modulation. Prog. Neuro Psychopharmacol. Biol. Psychiatry 76 (2017), 116–123, 10.1016/j.pnpbp.2017.03.004.
Gomez-Pilar, J., de Luis-García, R., Lubeiro, A., de la Red, H., Poza, J., Núñez, P., Molina, V., Relations between structural and EEG-based graph metrics in healthy controls and schizophrenia patients. Hum. Brain Mapp. 39:8 (2018), 3152–3165, 10.1002/hbm.24066.
Gomez-Pilar, J., de Luis-García, R., Lubeiro, A., de Uribe, N., Poza, J., Núñez, P., Molina, V., Deficits of entropy modulation in schizophrenia are predicted by functional connectivity strength in the theta band and structural clustering. Neuroimage 18 (2018), 382–389, 10.1016/j.nicl.2018.02.005.
Gomez-Pilar, J., Poza, J., Bachiller, A., Gómez, C., Núñez, P., Lubeiro, A., Hornero, R., Quantification of graph complexity based on the edge weight distribution balance: application to brain networks. Int. J. Neural Syst., 28(01), 2018, 1750032, 10.1142/S0129065717500320.
Gonzalez-Burgos, G., Fish, K.N., Lewis, D.A., GABA neuron alterations, cortical circuit dysfunction and cognitive deficits in schizophrenia. Neural Plast., 2011, 2011, 10.1155/2011/723184.
Kay, S.R., Fiszbein, A., Opler, L.A., The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13:2 (1987), 261–276 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/3616518.
Lachaux, J.P., Rodriguez, E., Martinerie, J., Varela, F.J., Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8:4 (1999), 194–208 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10619414.
Molina, V., Bachiller, A., Gomez-Pilar, J., Lubeiro, A., Hornero, R., Cea-Cañas, B., Poza, J., Deficit of entropy modulation of the EEG in schizophrenia associated to cognitive performance and symptoms. A replication study. Schizophr. Res. 195 (2018), 334–342, 10.1016/j.schres.2017.08.057.
Northoff, G., Beyond the passive/active dichotomy: a spectrum model of the brain's neural activities. The Spontaneous Brain, 2018, The MIT Press, 3–25, 10.7551/mitpress/11046.003.0004.
Núñez, P., Poza, J., Bachiller, A., Gomez-Pilar, J., Lubeiro, A., Molina, V., Hornero, R., Exploring non-stationarity patterns in schizophrenia: neural reorganization abnormalities in the alpha band. J. Neural Eng., 14(4), 2017, 046001, 10.1088/1741-2552/aa6e05.
Pomarol-Clotet, E., Salvador, R., Sarró, S., Gomar, J., Vila, F., Martínez, Á., McKenna, P.J., Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network?. Psychol. Med. 38:8 (2008), 1185–1193, 10.1017/S0033291708003565.
Pomarol-Clotet, E., Moro, N., Sarró, S., Goikolea, J.M., Vieta, E., Amann, B., Salvador, R., Failure of de-activation in the medial frontal cortex in mania: evidence for default mode network dysfunction in the disorder. World J. Biol. Psychiatr. 13:8 (2012), 616–626, 10.3109/15622975.2011.573808.
Rubinov, M., Knock, S.A., Stam, C.J., Micheloyannis, S., Harris, A.W.F., Williams, L.M., Breakspear, M., Small-world properties of nonlinear brain activity in schizophrenia. Hum. Brain Mapp. 30:2 (2009), 403–416, 10.1002/hbm.20517.
Segarra, N., Bernardo, M., Gutierrez, F., Justicia, A., Fernadez-Egea, E., Allas, M., Keefe, R.S.E., Spanish validation of the brief assessment in cognition in schizophrenia (BACS) in patients with schizophrenia and healthy controls. Eur. Psychiatr. 26:2 (2011), 69–73, 10.1016/j.eurpsy.2009.11.001.
Spencer, K.M., Nestor, P.G., Niznikiewicz, M.A., Salisbury, D.F., Shenton, M.E., McCarley, R.W., Abnormal neural synchrony in schizophrenia. J. Neurosci. 23:19 (2003), 7407–7411 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12917376.
Stam, C.J., van Straaten, E.C.W., The organization of physiological brain networks. Clin. Neurophysiol. 123:6 (2012), 1067–1087, 10.1016/j.clinph.2012.01.011.
Torrence, C., Compo, G.P., Torrence, C., Compo, G.P., A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79:1 (1998), 61–78, 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2.
Uhlhaas, P.J., Singer, W., Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11:2 (2010), 100–113, 10.1038/nrn2774.
van den Heuvel, M.P., Stam, C.J., Boersma, M., Hulshoff Pol, H.E., Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. NeuroImage 43:3 (2008), 528–539, 10.1016/j.neuroimage.2008.08.010.
van den Heuvel, M.P., Mandl, R.C.W., Stam, C.J., Kahn, R.S., Hulshoff Pol, H.E., Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J. Neurosci. 30:47 (2010), 15915–15926, 10.1523/JNEUROSCI.2874-10.2010.
van Diessen, E., Numan, T., van Dellen, E., van der Kooi, A.W., Boersma, M., Hofman, D., Stam, C.J., Opportunities and methodological challenges in EEG and MEG resting state functional brain network research. Clin. Neurophysiol. 126:8 (2015), 1468–1481, 10.1016/j.clinph.2014.11.018.
Varela, F., Lachaux, J.-P., Rodriguez, E., Martinerie, J., The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2:4 (2001), 229–239, 10.1038/35067550.
von Stein, A., Chiang, C., König, P., Top-down processing mediated by interareal synchronization. Proc. Natl. Acad. Sci. U. S. A. 97:26 (2000), 14748–14753, 10.1073/pnas.97.26.14748.
Whitfield-Gabrieli, S., Thermenos, H.W., Milanovic, S., Tsuang, M.T., Faraone, S.V., McCarley, R.W., Seidman, L.J., Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 106:4 (2009), 1279–1284, 10.1073/pnas.0809141106.