[en] Schizophrenia has been associated with a reduced task-related modulation of cortical activity assessed through electroencephalography (EEG). However, to the best of our knowledge, no study so far has assessed the underpinnings of this decreased EEG modulation in schizophrenia. A possible substrate of these findings could be a decreased inhibitory function, a replicated finding in the field. In this pilot study, our aim was to explore the association between EEG modulation during a cognitive task and the inhibitory system function in vivo in a sample including healthy controls and patients with schizophrenia. We hypothesized that the replicated decreased task-related activity modulation during a cognitive task in schizophrenia would be related to a hypofunction of the inhibitory system. For this purpose, 27 healthy controls and 22 patients with schizophrenia (including 13 first episodes) performed a 3-condition auditory oddball task from which the spectral entropy modulation was calculated. In addition, cortical reactivity-as an index of the inhibitory function-was assessed by the administration of 75 monophasic transcranial magnetic stimulation single pulses over the left dorsolateral prefrontal cortex. Our results replicated the task-related cortical activity modulation deficit in schizophrenia patients. Moreover, schizophrenia patients showed higher cortical reactivity following transcranial magnetic stimulation single pulses over the left dorsolateral prefrontal cortex compared to healthy controls. Cortical reactivity was inversely associated with EEG modulation, supporting the idea that a hypofunction of the inhibitory system could hamper the task-related modulation of EEG activity.
Disciplines :
Psychiatry
Author, co-author :
Fernández-Linsenbarth, Inés ; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005, Valladolid, Spain
Mijancos-Martínez, Gema ; Biomedical Engineering Research Centre (CREB), Department of Automatic Control (ESAII), Polytechnic University of Catalonia, Barcelona, Spain ; Institute of Research Sant Joan de Déu, Barcelona, Spain
Bachiller, Alejandro ; Biomedical Engineering Research Centre (CREB), Department of Automatic Control (ESAII), Polytechnic University of Catalonia, Barcelona, Spain ; Institute of Research Sant Joan de Déu, Barcelona, Spain
Nunez Novo, Pablo ; Université de Liège - ULiège > Département des sciences cliniques ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain ; Biomaterials and Nanomedicine (BICER-BBN), CIBER of Bioengineering, Madrid, Spain
Rodríguez-González, Víctor ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain ; Biomaterials and Nanomedicine (BICER-BBN), CIBER of Bioengineering, Madrid, Spain
Beño-Ruiz-de-la-Sierra, Rosa M ; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005, Valladolid, Spain
Roig-Herrero, Alejandro ; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005, Valladolid, Spain ; Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain
Arjona-Valladares, Antonio ; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005, Valladolid, Spain
Poza, Jesús ; Biomedical Engineering Group, University of Valladolid, Valladolid, Spain ; Biomaterials and Nanomedicine (BICER-BBN), CIBER of Bioengineering, Madrid, Spain ; Instituto de Investigación en Matemáticas (IMUCA), University of Valladolid, Valladolid, Spain
Mañanas, Miguel Ángel ; Biomedical Engineering Research Centre (CREB), Department of Automatic Control (ESAII), Polytechnic University of Catalonia, Barcelona, Spain ; Institute of Research Sant Joan de Déu, Barcelona, Spain ; Biomaterials and Nanomedicine (BICER-BBN), CIBER of Bioengineering, Madrid, Spain
Molina, Vicente ; Psychiatry Department, School of Medicine, University of Valladolid, Av. Ramón y Cajal, 7, 47005, Valladolid, Spain. vicente.molina@uva.es ; Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain. vicente.molina@uva.es ; Neurosciences Institute of Castilla y Léon (INCYL), University of Salamanca, Salamanca, Spain. vicente.molina@uva.es
Language :
English
Title :
Relation between task-related activity modulation and cortical inhibitory function in schizophrenia and healthy controls: a TMS-EEG study.
Publication date :
June 2024
Journal title :
European Archives of Psychiatry and Clinical Neuroscience
ISSN :
0940-1334
eISSN :
1433-8491
Publisher :
Springer Science and Business Media Deutschland GmbH, Germany
ISCIII - Instituto de Salud Carlos III MICINN - Ministerio de Ciencia e Innovacion Fundació la Marató de TV3 AGAUR - Agència de Gestió d'Ajuts Universitaris i de Recerca UVA - Universidad de Valladolid
Funding text :
Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This study has been supported by the “Gerencia Regional de Salud de Castilla y León” (grant IDs GRS 2029/A/19, GRS 2121/A/2020, and GRS 2487/A/22), “Instituto de Salud Carlos III” (grant ID PI22/00465), and partially supported by the “Ministerio de Ciencia e Innovación (MICINN)” (grant ID PID2020-117751RB-I00), and “Fundació La Marató de TV3” (grant ID 202219–30-31). IFL and RMBRS are in receipt of predoctoral grants from the “Consejería de Educación, Junta de Castilla y León” (Spain) and the European Social Fund (grant IDs VA-183–18 and VA-223–19, respectively). GMM is in receipt of a FI-2022 grant from “Agència de Gestió d'Ajuts Universitaris i de Recerca (AGAUR)”, and AB is a Serra Húnter Fellow. Funding sources had no other role than financial support providers.
G. Buzsáki A. Draguhn Neuronal olscillations in cortical networks Science 2004 80 304 1926 1929 10.1126/science.1099745
F. Varela J.P. Lachaux E. Rodriguez J. Martinerie The brainweb: phase synchronization and large-scale integration Nat Rev Neurosci 2001 2 229 239 1:CAS:528:DC%2BD3MXis1yqu74%3D 10.1038/35067550 11283746
G.M. Edelman Wider than the sky. The phenomenal gift of consciousness 2004 New Haven Yale University Press
S. Dehaene J.P. Changeux Experimental and theoretical approaches to conscious processing Neuron 2011 70 200 227 1:CAS:528:DC%2BC3MXlsFWqtr8%3D 10.1016/j.neuron.2011.03.018 21521609
S. Dehaene M. Kerszberg J.P. Changeux A neuronal model of a global workspace in effortful cognitive tasks Proc Natl Acad Sci USA 1998 95 14529 14534 1:CAS:528:DyaK1cXns1Gltro%3D 10.1073/pnas.95.24.14529 9826734 24407
S. Dehaene J.P. Changeux L. Naccache et al. Conscious, preconscious, and subliminal processing: a testable taxonomy Trends Cogn Sci 2006 10 204 211 10.1016/j.tics.2006.03.007 16603406
G. Buzsáki Diversity of cortical functions: inhibiton, ryhtms of the brain 2006 New York Oxford University Press
G. Gonzalez-Burgos K.N. Fish D.A. Lewis GABA neuron alterations, cortical circuit dysfunction and cognitive deficits in schizophrenia Neural Plast 2011 10.1155/2011/723184 22164341 3216374
D.A. Lewis K.N. Fish D. Arion G.-B. Guillermo Perisomatic inhibition and cortical circuit dysfunction in schizophrenia Curr Opin Neurobiol 2011 21 866 872 1:CAS:528:DC%2BC38XlsFSlsw%3D%3D 10.1016/j.conb.2011.05.013 21680173 3183273
C. Fee M. Banasr E. Sibille Somatostatin-positive GABA interneuron deficits in depression: cortical microcircuit and therapeutic perspectives Biol Psychiatry 2017 82 549 559 1:CAS:528:DC%2BC2sXhtFGiu73L 10.1016/j.biopsych.2017.05.024 28697889 5610074
J. Gomez-Pilar R. de Luis-García A. Lubeiro et al. Relations between structural and EEG-based graph metrics in healthy controls and schizophrenia patients Hum Brain Mapp 2018 39 3152 3165 10.1002/hbm.24066 29611297 6866568
A. Bachiller A. Díez V. Suazo et al. Decreased spectral entropy modulation in patients with schizophrenia during a P300 task Eur Arch Psychiatry Clin Neurosci 2014 264 533 543 10.1007/s00406-014-0488-6 24496581
V. Molina A. Bachiller J. Gomez-Pilar et al. Deficit of entropy modulation of the EEG in schizophrenia associated to cognitive performance and symptoms. A replication study Schizophr Res 2018 195 334 342 10.1016/j.schres.2017.08.057 28886890
V. Molina A. Lubeiro R. de Luis-García J. Gómez-Pilar Deficit of entropy modulation of the EEG: a biomarker for the altered function in schizophrenia and bipolar disorder? J Neuropsychiatry Clin Neurosci 2020 45 322
B. Cea-Cañas J. Gomez-Pilar P. Núñez et al. Connectivity strength of the EEG functional network in schizophrenia and bipolar disorder Prog Neuro Psychopharmacol Biol Psychiatry 2020 98 1:CAS:528:DC%2BC1MXitFOrurrE 10.1016/j.pnpbp.2019.109801
J. Gomez-Pilar R. de Luis-García A. Lubeiro et al. Deficits of entropy modulation in schizophrenia are predicted by functional connectivity strength in the theta band and structural clustering NeuroImage Clin 2018 18 382 389 10.1016/j.nicl.2018.02.005 29487795 5814380
M. Iglesias-Tejedor Á. Díez V. Llorca-Bofí et al. Relation between EEG resting-state power and modulation of P300 task-related activity in theta band in schizophrenia Prog Neuro Psychopharmacol Biol Psychiatry 2022 10.1016/j.pnpbp.2022.110541
B.P. Blum J.J. Mann The GABAergic system in schizophrenia Int J Neuropsychopharmacol 2002 5 159 179 1:CAS:528:DC%2BD3sXnsVCjsr0%3D 10.1017/S1461145702002894 12135541
V. Kumar B. Vajawat N.P. Rao Frontal GABA in schizophrenia: a meta-analysis of 1H-MRS studies World J Biol Psychiatry 2021 22 1 13 1:CAS:528:DC%2BB38XpsFChs7c%3D 10.1080/15622975.2020.1731925 32067569
S. Tremblay N.C. Rogasch I. Premoli et al. Clinical utility and prospective of TMS–EEG Clin Neurophysiol 2019 130 802 844 10.1016/j.clinph.2019.01.001 30772238
X. Du L.M. Rowland A. Summerfelt et al. TMS evoked N100 reflects local GABA and glutamate balance Physiol Behav 2018 176 139 148 10.1016/j.brs.2018.05.002.TMS
F. Ferrarelli B.A. Riedner M.J. Peterson G. Tononi Altered prefrontal activity and connectivity predict different cognitive deficits in schizophrenia Hum Brain Mapp 2015 36 4539 4552 10.1002/hbm.22935 26288380 6869713
P.B. Fitzgerald T.L. Brown N.A.U. Marston et al. A transcranial magnetic stimulation study of abnormal cortical inhibition in schizophrenia Psychiatry Res 2003 118 197 207 10.1016/S0165-1781(03)00094-5 12834814
F. Farzan M.S. Barr W. Wong et al. Suppression of γ-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study Neuropsychopharmacology 2009 34 1543 1551 1:CAS:528:DC%2BD1MXksFaguro%3D 10.1038/npp.2008.211 19037204
F. Farzan M.S. Barr A.J. Levinson et al. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia Brain 2010 133 1505 1514 10.1093/brain/awq046 20350936
Y. Noda M.S. Barr R. Zomorrodi et al. Evaluation of short interval cortical inhibition and intracortical facilitation from the dorsolateral prefrontal cortex in patients with schizophrenia Sci Rep 2017 10.1038/s41598-017-17052-3 29213090 5719013
N. Radhu L.G. Dominguez F. Farzan et al. Evidence for inhibitory deficits in the prefrontal cortex in schizophrenia Brain 2015 138 483 497 10.1093/brain/awu360 25524710
S. Groppa A. Oliviero A. Eisen et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee Clin Neurophysiol 2012 123 858 882 1:STN:280:DC%2BC38vjsFKqtw%3D%3D 10.1016/j.clinph.2012.01.010 22349304 4890546
P.B. Fitzgerald J.J. Maller K.E. Hoy et al. Exploring the optimal site for the localization of dorsolateral prefrontal cortex in brain stimulation experiments Brain Stimul 2009 2 234 237 10.1016/j.brs.2009.03.002 20633422
P.M. Rusjan M.S. Barr F. Farzan et al. Optimal transcranial magnetic stimulation coil placement for targeting the dorsolateral prefrontal cortex using novel magnetic resonance image-guided neuronavigation Hum Brain Mapp 2010 31 1643 1652 10.1002/hbm.20964 20162598 6871247
N.C. Rogasch Z.J. Daskalakis P.B. Fitzgerald Cortical inhibition of distinct mechanisms in the dorsolateral prefrontal cortex is related to working memory performance: a TMS-EEG study Cortex 2015 64 68 77 10.1016/j.cortex.2014.10.003 25461708
C. Bledowski D. Prvulovic K. Hoechstetter et al. Behavioral/systems/cognitive localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study J Neurosci 2004 10.1523/JNEUROSCI.1897-04.2004 15496671 6730097
P. Núñez J. Poza A. Bachiller et al. Exploring non-stationarity patterns in schizophrenia: neural reorganization abnormalities in the alpha band-PubMed J Neural Eng 2017 14 046001 10.1088/1741-2552/aa6e05 28424430
R. Oostenveld P. Fries E. Maris J.M. Schoffelen FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data Comput Intell Neurosci 2011 10.1155/2011/156869 21822426 3148593
N.C. Rogasch R.H. Thomson F. Farzan et al. Removing artefacts from TMS-EEG recordings using independent component analysis: Importance for assessing prefrontal and motor cortex network properties Neuroimage 2014 101 425 439 10.1016/j.neuroimage.2014.07.037 25067813
Cline C, Lucas M, Sun Y, et al (2021) Advanced artifact removal for automated TMS-EEG data processing. Int. In: IEEE/EMBS Conf. Neural Eng. NER, pp 1039–1042
R.F.H. Cash Y. Noda R. Zomorrodi et al. Characterization of glutamatergic and GABA A-mediated neurotransmission in motor and dorsolateral prefrontal cortex using paired-pulse TMS-EEG Neuropsychopharmacology 2017 42 502 511 1:CAS:528:DC%2BC28Xhtlyqs7vL 10.1038/npp.2016.133 27461082
E. Bramon S. Rabe-Hesketh P. Sham et al. Meta-analysis of the P300 and P50 waveforms in schizophrenia Schizophr Res 2004 70 315 329 10.1016/j.schres.2004.01.004 15329307
J.L. Santos E.M. Sánchez-Morla A. Aparicio et al. P50 gating in deficit and nondeficit schizophrenia Schizophr Res 2010 119 183 190 10.1016/j.schres.2010.01.010 20153607
Z.J. Daskalakis P.B. Fitzgerald B.K. Christensen The role of cortical inhibition in the pathophysiology and treatment of schizophrenia Brain Res Rev 2007 56 427 442 1:CAS:528:DC%2BD2sXhsVSrsrzM 10.1016/j.brainresrev.2007.09.006 17980435
N. Radhu L.G. Dominguez T.A. Greenwood et al. Investigating cortical inhibition in first-degree relatives and probands in schizophrenia Sci Rep 2017 7 43629 10.1038/srep43629 28240740 5378912
Z.J. Daskalakis B.K. Christensen R. Chen et al. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation Arch Gen Psychiatry 2002 59 347 354 10.1001/archpsyc.59.4.347 11926935
I. Fernández-Linsenbarth Á. Planchuelo-Gómez Á. Díez et al. Neurobiological underpinnings of cognitive subtypes in psychoses: a cross-diagnostic cluster analysis Schizophr Res 2021 229 102 111 10.1016/j.schres.2020.11.013 33221149
B.A. Clementz D.A. Parker R.L. Trotti et al. Psychosis biotypes: replication and validation from the B-SNIP consortium Schizophr Bull 2022 48 56 68 10.1093/schbul/sbab090 34409449
P. Canali G. Sferrazza Papa A.G. Casali et al. Changes of cortical excitability as markers of antidepressant response in bipolar depression: preliminary data obtained by combining transcranial magnetic stimulation (TMS) and electroencephalography (EEG) Bipolar Disord 2014 16 809 819 10.1111/bdi.12249 25219396
D. Voineskos D.M. Blumberger R. Zomorrodi et al. Altered transcranial magnetic stimulation-electroencephalographic markers of inhibition and excitation in the dorsolateral prefrontal cortex in major depressive disorder Biol Psychiatry 2019 85 477 486 10.1016/j.biopsych.2018.09.032 30503506
P. Dhami S. Atluri J.C. Lee et al. Prefrontal cortical reactivity and connectivity markers distinguish youth depression from healthy youth Cereb Cortex 2020 30 3884 3894 10.1093/CERCOR/BHAA004 32118262 7264684
C. Ritter A. Buchmann S.T. Müller et al. Evaluation of prefrontal γ-aminobutyric acid and glutamate levels in individuals with major depressive disorder using proton magnetic resonance spectroscopy JAMA Psychiat 2022 79 1209 1216 10.1001/JAMAPSYCHIATRY.2022.3384
