[en] There is some consistency in previous EEG findings that patients with schizophrenia have increased resting-state cortical activity. Furthermore, in previous work, we have provided evidence that there is a deficit in the modulation of bioelectrical activity during the performance of a P300 task in schizophrenia. Our hypothesis here is that a basal hyperactivation would be related with altered ability to change or modulate cortical activity during a cognitive task. However, no study so far, to the best of our knowledge, has studied the association between resting-state activity and task-related modulation. With this aim, we used a dual EEG paradigm (resting state and oddball task for elicitation of the P300 evoked potential) in a sample of patients with schizophrenia (n = 100), which included a subgroup of patients with first episode psychosis (n = 30), as well as a group of healthy controls (n = 93). The study measures were absolute power for resting-state; and spectral entropy (SE) and connectivity strength (CS) for P300-task data, whose modulation had been previously found to be altered in schizophrenia. Following the literature on P300, we focused our study on the theta frequency band. As expected, our results showed an increase in resting state activity and altered task-related modulation. Moreover, we found an inverse relationship between the amount of resting-state activity and modulation of task-related activity. Our results confirm our hypothesis and support the idea that a greater amount of resting theta-band synchrony could hamper the modulation of signal regularity (quantified by SE) and activity density (measured by CS) during the P300 task performance. This association was found in both patients and controls, suggesting the existence of a common mechanism and a possible ceiling effect in schizophrenia patients in relation to a decreased inhibitory function that limits their cortical reactivity to the task.
Disciplines :
Psychiatry
Author, co-author :
Iglesias-Tejedor, María; Clinical Neurophysiology Service, Clinical University Hospital of Valladolid, Valladolid, Spain. Electronic address: maria29it@gmail.com
Díez, Álvaro; Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain. Electronic address: a.diez@uva.es
Nunez Novo, Pablo ; Université de Liège - ULiège > GIGA > GIGA Consciousness - Coma Science Group ; University of Valladolid > Biomedical Engineering Group
Castaño-Díaz, Carolina; Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain. Electronic address: carolina.castano@salud.madrid.org
Bote, Berta; Psychiatry Service, University Hospital of Salamanca, Salamanca, Spain. Electronic address: bbote@saludcastillayleon.es
Sanz-Fuentenebro, Javier; Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain. Electronic address: javier.sanz@salud.madrid.org
Molina, Vicente; Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain, Psychiatry Service, University Hospital of Valladolid, Valladolid, Spain, Neuroscience Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain. Electronic address: vicente.molina@uva.es
Language :
English
Title :
Relation between EEG resting-state power and modulation of P300 task-related activity in theta band in schizophrenia.
Publication date :
08 June 2022
Journal title :
Progress in Neuro-Psychopharmacology and Biological Psychiatry
This study has been supported by the 'Gerencia Regional de Salud de Castilla y Leon' ( GRS 2121/A/2020 ) and the 'Instituto de Salud Carlos III' ( PI 18/00178 ) grants.
Bachiller, A., Díez, Á., Suazo, V., Domínguez, C., Ayuso, M., Hornero, R., Poza, J., Molina, V., Díez, A., Suazo, V., Domínguez, C., Ayuso, M., Hornero, R., Poza, J., Molina, V., Decreased spectral entropy modulation in patients with schizophrenia during a P300 task. Eur. Arch. Psychiatry Clin. Neurosci. 264:6 (2014), 1–11, 10.1007/s00406-014-0488-6.
Bachiller, A., Lubeiro, A., Díez, Á., Suazo, V., Dominguez, C., Blanco, J.A.A., Ayuso, M., Hornero, R., Poza, J., Molina, V., Domínguez, C., Blanco, J.A.A., Ayuso, M., Hornero, R., Poza, J., Molina, V., Decreased entropy modulation of EEG response to novelty and relevance in schizophrenia during a P300 task. Eur. Arch. Psychiatry Clin. Neurosci., 265(6), 2014, 10.1007/s00406-014-0525-5.
Bachiller, Alejandro, Poza, J., Gomez, C., Molina, V., Suazo, V., Hornero, R., 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, 16007, 10.1088/1741-2560/12/1/016007.
Başar-Eroglu, C., Başar, E., Demiralp, T., Schürmann, M., P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. Int. J. Psychophysiol., 13(2), 1992, 10.1016/0167-8760(92)90055-G.
Bledowski, C., Prvulovic, D., Hoechstetter, K., Scherg, M., Wibral, M., Goebel, R., Linden, D.E., 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 24/42/9353 [pii] https://doi.org/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, 10.1016/j.neulet.2008.09.055.
Buzsáki, G., Diversity of cortical functions: inhibition. Rythms of the Brain, 2006, Oxford University Press, 61–79.
Cea-Cañas, B., Gomez-Pilar, J., Núñez, P., Rodríguez-Vázquez, E., de Uribe, N., Díez, Á., Pérez-Escudero, A., Molina, V., Connectivity strength of the EEG functional network in schizophrenia and bipolar disorder. Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 98, 2020, 109801, 10.1016/j.pnpbp.2019.109801.
Cole, M.W., Bassett, D.S., Power, J.D., Braver, T.S., Petersen, S.E., Intrinsic and task-evoked network architectures of the human brain. Neuron, 83(1), 2014, 10.1016/j.neuron.2014.05.014.
Delorme, A., Makeig, S., EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods, 134(1), 2004, 10.1016/j.jneumeth.2003.10.009.
Díez, Á., Suazo, V., Casado, P., Martín-Loeches, M., Molina, V., Martin-Loeches, M., Molina, V., Díez, A., Suazo, V., Casado, P., Martín-Loeches, M., Molina, V., Spatial distribution and cognitive correlates of gamma noise power in schizophrenia. Psychol. Med. 43:September (2013), 1–11, 10.1017/S0033291712002103.
Doege, K., Bates, A.T., White, T.P., Das, D., Boks, M.P., Liddle, P.F., Reduced event-related low frequency EEG activity in schizophrenia during an auditory oddball task. Psychophysiology 46:3 (2009), 566–577, 10.1111/j.1469-8986.2009.00785.x.
Garakh, Z., Zaytseva, Y., Kapranova, A., Fiala, O., Horacek, J., Shmukler, A., Gurovich, I.Y., Strelets, V.B., EEG correlates of a mental arithmetic task in patients with first episode schizophrenia and schizoaffective disorder. Clin. Neurophysiol. 126:11 (2015), 2090–2098, 10.1016/j.clinph.2014.12.031.
Gomez-Pilar, J., de Luis-García, R., Lubeiro, A., de Uribe, N., Poza, J., Núñez, P., Ayuso, M., Hornero, R., Molina, V., Deficits of entropy modulation in schizophrenia are predicted by functional connectivity strength in the theta band and structural clustering. NeuroImage. Clin. 18 (2018), 382–389, 10.1016/j.nicl.2018.02.005.
Hanslmayr, S., Backes, H., Straub, S., Popov, T., Langguth, B., Hajak, G., Bäuml, K.H.T., Landgrebe, M., Enhanced resting-state oscillations in schizophrenia are associated with decreased synchronization during inattentional blindness. Hum. Brain Mapp. 34:9 (2013), 2266–2275, 10.1002/hbm.22064.
Li, F., Liu, T., Wang, F., Li, H., Gong, D., Zhang, R., Jiang, Y., Tian, Y., Guo, D., Yao, D., Xu, P., Relationships between the resting-state network and the P3: evidence from a scalp EEG study. Sci. Rep., 5, 2015, 10.1038/srep15129.
Manoach, D.S., Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 60:2–3 (2003), 285–298 S0920996402002943 [pii].
Molina, V., Bachiller, A., Suazo, V., Lubeiro, A., Poza, J.J., Hornero, R., Noise power associated with decreased task-induced variability of brain electrical activity in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 266:1 (2016), 55–61, 10.1007/s00406-014-0569-6.
Molina, V., Bachiller, A., Gomez-Pilar, J., Lubeiro, A., Hornero, R., Cea-Cañas, B., Valcárcel, C., Haidar, M.K., 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.
Molina, V., Lubeiro, A., de Luis Garcia, R., Gomez-Pilar, J., Martín-Santiago, O., Iglesias-Tejedor, M., Holgado-Madera, P., Segarra-Echeverría, R., Recio-Barbero, M., Núñez, P., Haidar, M.K., Fernández-Sevillano, J., Sanz-Fuentenebro, J., Deficits of entropy modulation of the EEG: a biomarker for altered function in schizophrenia and bipolar disorder?. J. Psychiatry Neurosci., 45(5), 2020, 10.1503/jpn.190032.
Newson, J.J., Thiagarajan, T.C., EEG frequency bands in psychiatric disorders: a review of resting state studies. Front. Hum. Neurosci. 12:January (2019), 1–24, 10.3389/fnhum.2018.00521.
Northoff, G., Gomez-Pilar, J., Overcoming rest-task divide-abnormal Temporospatial dynamics and its cognition in schizophrenia. Schizophr. Bull. 47:3 (2021), 751–765, 10.1093/schbul/sbaa178.
Northoff, G., Huang, Z., How do the brain's time and space mediate consciousness and its different dimensions? Temporo-spatial theory of consciousness (TTC). In. Neurosci. Biobehav. Rev., 80, 2017, 10.1016/j.neubiorev.2017.07.013.
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, 46001, 10.1088/1741-2552/aa6e05.
Rogala, J., Kublik, E., Krauz, R., Wróbel, A., Resting-state EEG activity predicts frontoparietal network reconfiguration and improved attentional performance. Sci. Rep., 10(1), 2020, 10.1038/s41598-020-61866-7.
Scheeringa, R., Fries, P., Petersson, K.M., Oostenveld, R., Grothe, I., Norris, D.G., Hagoort, P., Bastiaansen, M.C., Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 69:3 (2011), 572–583 S0896-6273(10)01081-0 [pii] https://doi.org/10.1016/j.neuron.2010.11.044.
Soltani, M., Knight, R.T., Yamaguchi, S., Chao, L.L., Nielsen-Bohlman, L., Neural origins of the P300. Crit. Rev. Neurobiol. 14:3–4 (2000), 199–224.
Spencer, K.M., Polich, J., Poststimulus EEG spectral analysis and P300: attention, task, and probability. Psychophysiology, 36(2), 1999, 10.1017/S0048577299971615.
Suazo, V., Díez, T., Martín, C., Ballesteros, A., Casado, P., Martín-Loeches, M., Molina, V., Díez, Á., Martín, C., Ballesteros, A., Casado, P., Martín-Loeches, M., Molina, V., Elevated noise power in gamma band related to negative symptoms and memory deficit in schizophrenia. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 38:2 (2012), 270–275, 10.1016/j.pnpbp.2012.04.010.
von Stein, A., Chiang, C., Konig, 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 97/26/14748.
Winterer, G., Ziller, M., Dorn, H., Frick, K., Mulert, C., Wuebben, Y., Herrmann, W.M., Coppola, R., Schizophrenia: reduced signal-to-noise ratio and impaired phase-locking during information processing. Clin. Neurophysiol. 111:5 (2000), 837–849 S1388-2457(99)00322-3 [pii].
Womelsdorf, T., Schoffelen, J.M., Oostenveld, R., Singer, W., Desimone, R., Engel, A.K., Fries, P., Modulation of neuronal interactions through neuronal synchronization. Science 316:5831 (2007), 1609–1612, 10.1126/science.1139597 316/5831/1609 [pii].
