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Research Paper

Deficits of entropy modulation of the EEG: A biomarker for altered function in schizophrenia and bipolar disorder?

Vicente Molina, Alba Lubeiro, Rodrigo de Luis Garcia, Javier Gomez-Pilar, Oscar Martín-Santiago, María Iglesias-Tejedor, Pedro Holgado-Madera, Rafael Segarra-Echeverría, María Recio-Barbero, Pablo Núñez, Mahmoud Karim Haidar, Jessica Fernández-Sevillano and Javier Sanz-Fuentenebro
J Psychiatry Neurosci September 01, 2020 45 (5) 322-333; DOI: https://doi.org/10.1503/jpn.190032
Vicente Molina
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Alba Lubeiro
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Rodrigo de Luis Garcia
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Javier Gomez-Pilar
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Oscar Martín-Santiago
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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María Iglesias-Tejedor
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Pedro Holgado-Madera
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Rafael Segarra-Echeverría
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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María Recio-Barbero
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Pablo Núñez
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Mahmoud Karim Haidar
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Jessica Fernández-Sevillano
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Javier Sanz-Fuentenebro
From the Psychiatry Department, School of Medicine, University of Valladolid, Valladolid, Spain (Molina, Lubeiro); the Psychiatry Service, Clinical Hospital of Valladolid, Valladolid, Spain (Molina, Martín-Santiago); the Neurosciences Institute of Castilla y León (INCYL), University of Salamanca, Salamanca, Spain (Molina); the Imaging Processing Laboratory, University of Valladolid, Valladolid, Spain (de Luis Garcia); the Biomedical Engineering Group, University of Valladolid, Valladolid, Spain (Gomez-Pilar, Núñez); the Neurophysiology Service, Clinical Hospital of Valladolid, Valladolid, Spain (Iglesias-Tejedor); the Psychiatry Service, Doce de Octubre University Hospital, Madrid, Spain (Holgado-Madera, Sanz-Fuentenebro); the Psychiatry Service, Cruces Hospital, Bilbao, Spain (Segarra-Echeverría, Recio-Barbero); and the Psychiatry Service, Santiago Apostol Hospital, Vitoria, Spain (Haidar, Fernández-Sevillano)
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Abstract

Background: The synchronized activity of distributed neural assemblies — reflected in the electroencephalogram (EEG) — underpins mental function. In schizophrenia, modulation deficits of EEG spectral content during a P300 task have been replicated. The effects of treatment, chronicity and specificity in these deficits and their possible relationship with anatomic connectivity remain to be explored.

Methods: We assessed spectral entropy modulation of the EEG during a P300 task in 79 patients with schizophrenia (of those, 31 were in their first episode), 29 patients with bipolar disorder and 48 healthy controls. Spectral entropy values summarize EEG characteristics by quantifying the irregularity of spectral content. In a subsample, we calculated the network architecture of structural connectivity using diffusion tensor imaging and graph-theory parameters.

Results: We found significant spectral entropy modulation deficits with task performance in patients with chronic or first-episode schizophrenia and in patients with bipolar disorder, without significant pre-stimulus spectral entropy differences. The deficits were unrelated to treatment doses, and spectral entropy modulation did not differ between patients taking or not taking antipsychotics, lithium, benzodiazepines or antidepressants. Structural connectivity values were unrelated to spectral entropy modulation. In patients with schizophrenia, spectral entropy modulation was inversely related to negative symptoms and directly related to verbal memory.

Limitations: All patients were taking medication. Patients with bipolar disorder were euthymic and chronic. The cross-sectional nature of this study prevented a more thorough analysis of state versus trait criteria for spectral entropy changes.

Conclusion: Spectral entropy modulation with task performance is decreased in patients with schizophrenia and bipolar disorder. This deficit was not an effect of psychopharmacological treatment or structural connectivity and might reflect a deficit in the synchronization of the neural assemblies that underlie cognitive activity.

  • Received February 14, 2019.
  • Revision received September 30, 2019.
  • Accepted November 17, 2019.
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Journal of Psychiatry and Neuroscience: 45 (5)
J Psychiatry Neurosci
Vol. 45, Issue 5
1 Sep 2020
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Deficits of entropy modulation of the EEG: A biomarker for altered function in schizophrenia and bipolar disorder?
Vicente Molina, Alba Lubeiro, Rodrigo de Luis Garcia, Javier Gomez-Pilar, Oscar Martín-Santiago, María Iglesias-Tejedor, Pedro Holgado-Madera, Rafael Segarra-Echeverría, María Recio-Barbero, Pablo Núñez, Mahmoud Karim Haidar, Jessica Fernández-Sevillano, Javier Sanz-Fuentenebro
J Psychiatry Neurosci Sep 2020, 45 (5) 322-333; DOI: 10.1503/jpn.190032

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Deficits of entropy modulation of the EEG: A biomarker for altered function in schizophrenia and bipolar disorder?
Vicente Molina, Alba Lubeiro, Rodrigo de Luis Garcia, Javier Gomez-Pilar, Oscar Martín-Santiago, María Iglesias-Tejedor, Pedro Holgado-Madera, Rafael Segarra-Echeverría, María Recio-Barbero, Pablo Núñez, Mahmoud Karim Haidar, Jessica Fernández-Sevillano, Javier Sanz-Fuentenebro
J Psychiatry Neurosci Sep 2020, 45 (5) 322-333; DOI: 10.1503/jpn.190032
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