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Spontaneous neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

View ORCID ProfileLuca Iemi, Laura Gwilliams, Jason Samaha, Ryszard Auksztulewicz, Yael M Cycowicz, Jean-Remi King, Vadim V Nikulin, Thomas Thesen, Werner Doyle, Orrin Devinsky, Charles E Schroeder, Lucia Melloni, Saskia Haegens
doi: https://doi.org/10.1101/2021.03.01.433450
Luca Iemi
1Department of Psychiatry, Columbia University, College of Physicians and Surgeons, New York, NY, USA
2New York State Psychiatric Institute, New York, NY, USA
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  • ORCID record for Luca Iemi
  • For correspondence: luca.iemi@gmail.com
Laura Gwilliams
3Department of Neurological Surgery, University of California, San Francisco, CA, USA
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Jason Samaha
4Department of Psychology, University of California, Santa Cruz, Santa Cruz, USA
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Ryszard Auksztulewicz
5Department of Neuroscience, Max Planck Institute for Empirical Aesthetics, Frankfurt am Main, Germany
6Department of Neuroscience, City University of Hong Kong, Hong Kong, China
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Yael M Cycowicz
1Department of Psychiatry, Columbia University, College of Physicians and Surgeons, New York, NY, USA
2New York State Psychiatric Institute, New York, NY, USA
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Jean-Remi King
7Laboratoire des Systèmes Perceptifs, Département d’Études Cognitives, École Normale Supérieure, PSL University, CNRS, Paris, France
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Vadim V Nikulin
8Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
9Center for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russia
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Thomas Thesen
10Department of Neurology, New York University Langone Medical Center, New York City, USA
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Werner Doyle
10Department of Neurology, New York University Langone Medical Center, New York City, USA
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Orrin Devinsky
10Department of Neurology, New York University Langone Medical Center, New York City, USA
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Charles E Schroeder
1Department of Psychiatry, Columbia University, College of Physicians and Surgeons, New York, NY, USA
11Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY, USA
12Translational Neuroscience Division of the Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute, Orangeburg, NY, USA
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Lucia Melloni
5Department of Neuroscience, Max Planck Institute for Empirical Aesthetics, Frankfurt am Main, Germany
10Department of Neurology, New York University Langone Medical Center, New York City, USA
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Saskia Haegens
1Department of Psychiatry, Columbia University, College of Physicians and Surgeons, New York, NY, USA
2New York State Psychiatric Institute, New York, NY, USA
13Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, The Netherlands
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Abstract

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Spontaneous fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on invasive electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 02, 2021.
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Spontaneous neural oscillations influence behavior and sensory representations by suppressing neuronal excitability
Luca Iemi, Laura Gwilliams, Jason Samaha, Ryszard Auksztulewicz, Yael M Cycowicz, Jean-Remi King, Vadim V Nikulin, Thomas Thesen, Werner Doyle, Orrin Devinsky, Charles E Schroeder, Lucia Melloni, Saskia Haegens
bioRxiv 2021.03.01.433450; doi: https://doi.org/10.1101/2021.03.01.433450
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Spontaneous neural oscillations influence behavior and sensory representations by suppressing neuronal excitability
Luca Iemi, Laura Gwilliams, Jason Samaha, Ryszard Auksztulewicz, Yael M Cycowicz, Jean-Remi King, Vadim V Nikulin, Thomas Thesen, Werner Doyle, Orrin Devinsky, Charles E Schroeder, Lucia Melloni, Saskia Haegens
bioRxiv 2021.03.01.433450; doi: https://doi.org/10.1101/2021.03.01.433450

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