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Theta-phase dependent neuronal coding during sequence learning in human single neurons

Leila Reddy, Matthew W. Self, Benedikt Zoefel, Marlène Poncet, Jessy K. Possel, Judith C. Peters, Johannes C. Baayen, Sander Idema, Rufin VanRullen, Pieter R. Roelfsema
doi: https://doi.org/10.1101/630095
Leila Reddy
1Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, 31052, Toulouse, France
2CNRS, UMR 5549, Faculté de Médecine de Purpan, 31052 Toulouse, France
3Artificial and Natural Intelligence Toulouse Institute (ANITI), 31052 Toulouse, France
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  • For correspondence: leila.reddy@cnrs.fr
Matthew W. Self
4Department of Vision and Cognition, Netherlands Institute for Neuroscience (KNAW), 1105 BA, Amsterdam, The Netherlands
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Benedikt Zoefel
1Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, 31052, Toulouse, France
2CNRS, UMR 5549, Faculté de Médecine de Purpan, 31052 Toulouse, France
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Marlène Poncet
1Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, 31052, Toulouse, France
2CNRS, UMR 5549, Faculté de Médecine de Purpan, 31052 Toulouse, France
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Jessy K. Possel
4Department of Vision and Cognition, Netherlands Institute for Neuroscience (KNAW), 1105 BA, Amsterdam, The Netherlands
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Judith C. Peters
4Department of Vision and Cognition, Netherlands Institute for Neuroscience (KNAW), 1105 BA, Amsterdam, The Netherlands
5Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6200 MD Maastricht, The Netherlands
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Johannes C. Baayen
6Amsterdam University Medical Centers, location VUmc, Departments of Neurophysiology and Neurosurgery, Amsterdam, The Netherlands
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Sander Idema
6Amsterdam University Medical Centers, location VUmc, Departments of Neurophysiology and Neurosurgery, Amsterdam, The Netherlands
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Rufin VanRullen
1Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, 31052, Toulouse, France
2CNRS, UMR 5549, Faculté de Médecine de Purpan, 31052 Toulouse, France
3Artificial and Natural Intelligence Toulouse Institute (ANITI), 31052 Toulouse, France
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Pieter R. Roelfsema
4Department of Vision and Cognition, Netherlands Institute for Neuroscience (KNAW), 1105 BA, Amsterdam, The Netherlands
7Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081HV, Amsterdam, The Netherlands
8Psychiatry Department, Academic Medical Center, 1105 AZ Amsterdam, The Netherlands
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Abstract

The ability to maintain a sequence of items in short-term memory (STM) is a fundamental cognitive function. In the rodent hippocampus, the representation of sequentially organized spatial locations is reflected by the phase of action potentials relative to the theta oscillation (phase precession). We investigated whether the timing of neuronal activity relative to the theta brain oscillation also reflects sequence order in the medial temporal lobe of humans. We used a task in which human subjects learned sequences of pictures and recorded single neuron and local field potential activity with implanted electrodes. We report that spikes for three consecutive items in the sequence (the preferred stimulus for each cell, as well as the stimuli immediately preceding and following it) were phase-locked at distinct phases of the theta oscillation. Consistent with phase precession, spikes were fired at progressively earlier phases as the sequence advanced. These findings generalize previous findings in the rodent hippocampus to the human temporal lobe and suggest that encoding stimulus information at distinct oscillatory phases may play a role in maintaining their sequential order in STM.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • An issue was found in the previous version. This revision corrects it, and includes further control analyses.

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-ND 4.0 International license.
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Posted September 03, 2020.
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Theta-phase dependent neuronal coding during sequence learning in human single neurons
Leila Reddy, Matthew W. Self, Benedikt Zoefel, Marlène Poncet, Jessy K. Possel, Judith C. Peters, Johannes C. Baayen, Sander Idema, Rufin VanRullen, Pieter R. Roelfsema
bioRxiv 630095; doi: https://doi.org/10.1101/630095
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Theta-phase dependent neuronal coding during sequence learning in human single neurons
Leila Reddy, Matthew W. Self, Benedikt Zoefel, Marlène Poncet, Jessy K. Possel, Judith C. Peters, Johannes C. Baayen, Sander Idema, Rufin VanRullen, Pieter R. Roelfsema
bioRxiv 630095; doi: https://doi.org/10.1101/630095

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