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Articles, Systems/Circuits

Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation

Michael M. Plichta, Isabella Wolf, Sarah Hohmann, Sarah Baumeister, Regina Boecker, Adam J. Schwarz, Maria Zangl, Daniela Mier, Carsten Diener, Patric Meyer, Nathalie Holz, Matthias Ruf, Martin F. Gerchen, David Bernal-Casas, Vasil Kolev, Juliana Yordanova, Herta Flor, Manfred Laucht, Tobias Banaschewski, Peter Kirsch, Andreas Meyer-Lindenberg and Daniel Brandeis
Journal of Neuroscience 4 September 2013, 33 (36) 14526-14533; DOI: https://doi.org/10.1523/JNEUROSCI.0631-13.2013
Michael M. Plichta
1Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Departments of Psychiatry and Psychotherapy,
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Isabella Wolf
2Child and Adolescent Psychiatry and Psychotherapy,
5Neuroimaging, 68159 Mannheim, Germany,
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Sarah Hohmann
2Child and Adolescent Psychiatry and Psychotherapy,
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Sarah Baumeister
2Child and Adolescent Psychiatry and Psychotherapy,
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Regina Boecker
2Child and Adolescent Psychiatry and Psychotherapy,
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Adam J. Schwarz
6Tailored Therapeutics, Eli Lilly and Company, Indianapolis, Indiana 46285,
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Maria Zangl
1Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Departments of Psychiatry and Psychotherapy,
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Daniela Mier
3Clinical Psychology,
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Carsten Diener
4Cognitive and Clinical Neuroscience, and
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Patric Meyer
4Cognitive and Clinical Neuroscience, and
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Nathalie Holz
2Child and Adolescent Psychiatry and Psychotherapy,
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Matthias Ruf
5Neuroimaging, 68159 Mannheim, Germany,
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Martin F. Gerchen
3Clinical Psychology,
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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David Bernal-Casas
3Clinical Psychology,
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Vasil Kolev
8Bulgarian Academy of Sciences, Institute of Neurobiology, 1113 Sofia, Bulgaria,
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Juliana Yordanova
8Bulgarian Academy of Sciences, Institute of Neurobiology, 1113 Sofia, Bulgaria,
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Herta Flor
4Cognitive and Clinical Neuroscience, and
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Manfred Laucht
2Child and Adolescent Psychiatry and Psychotherapy,
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Tobias Banaschewski
2Child and Adolescent Psychiatry and Psychotherapy,
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Peter Kirsch
3Clinical Psychology,
7Bernstein-Center for Computational Neuroscience Heidelberg-Mannheim, 68159 Mannheim, Germany,
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Andreas Meyer-Lindenberg
1Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Departments of Psychiatry and Psychotherapy,
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Daniel Brandeis
2Child and Adolescent Psychiatry and Psychotherapy,
9Department of Child and Adolescent Psychiatry, University of Zurich, 8032 Zurich, Switzerland,
10Center for Integrative Human Physiology, University of Zurich, 8057 Zurich, Switzerland, and
11Neuroscience Center Zurich, University of Zurich and ETH Zurich, 8057 Zurich, Switzerland
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Abstract

Electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) have been used to study the neural correlates of reward anticipation, but the interrelation of EEG and fMRI measures remains unknown. The goal of the present study was to investigate this relationship in response to a well established reward anticipation paradigm using simultaneous EEG-fMRI recording in healthy human subjects. Analysis of causal interactions between the thalamus (THAL), ventral-striatum (VS), and supplementary motor area (SMA), using both mediator analysis and dynamic causal modeling, revealed that (1) THAL fMRI blood oxygenation level-dependent (BOLD) activity is mediating intermodal correlations between the EEG contingent negative variation (CNV) signal and the fMRI BOLD signal in SMA and VS, (2) the underlying causal connectivity network consists of top-down regulation from SMA to VS and SMA to THAL along with an excitatory information flow through a THAL→VS→SMA route during reward anticipation, and (3) the EEG CNV signal is best predicted by a combination of THAL fMRI BOLD response and strength of top-down regulation from SMA to VS and SMA to THAL. Collectively, these findings represent a likely neurobiological mechanism mapping a primarily subcortical process, i.e., reward anticipation, onto a cortical signature.

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The Journal of Neuroscience: 33 (36)
Journal of Neuroscience
Vol. 33, Issue 36
4 Sep 2013
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Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation
Michael M. Plichta, Isabella Wolf, Sarah Hohmann, Sarah Baumeister, Regina Boecker, Adam J. Schwarz, Maria Zangl, Daniela Mier, Carsten Diener, Patric Meyer, Nathalie Holz, Matthias Ruf, Martin F. Gerchen, David Bernal-Casas, Vasil Kolev, Juliana Yordanova, Herta Flor, Manfred Laucht, Tobias Banaschewski, Peter Kirsch, Andreas Meyer-Lindenberg, Daniel Brandeis
Journal of Neuroscience 4 September 2013, 33 (36) 14526-14533; DOI: 10.1523/JNEUROSCI.0631-13.2013

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Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation
Michael M. Plichta, Isabella Wolf, Sarah Hohmann, Sarah Baumeister, Regina Boecker, Adam J. Schwarz, Maria Zangl, Daniela Mier, Carsten Diener, Patric Meyer, Nathalie Holz, Matthias Ruf, Martin F. Gerchen, David Bernal-Casas, Vasil Kolev, Juliana Yordanova, Herta Flor, Manfred Laucht, Tobias Banaschewski, Peter Kirsch, Andreas Meyer-Lindenberg, Daniel Brandeis
Journal of Neuroscience 4 September 2013, 33 (36) 14526-14533; DOI: 10.1523/JNEUROSCI.0631-13.2013
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