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

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The ability to maintain a sequence of items in memory 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 participants learned a fixed sequence 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 sequential order in memory.

Original languageEnglish
Article number4839
JournalNature Communications
Volume12
Issue number1
DOIs
Publication statusPublished - Dec 2021

Bibliographical note

Funding Information:
We are grateful to C.J. Stam, E. van Dellen, L. Douw, P. Ris, S. Claus, D. Velis, and R. Joosten for help with obtaining ethics approval and for technical help with the patients and recordings. This work was supported by grants from the French Agence Nationale de la Recherche (ANR-12-JSH2-0004-01 and ANR AI-REPS–18-CE37-0007-01), the Fyssen foundation, and the Université Paul Sabatier, Toulouse, France (BQR, 2009 and Appel à Projets de Recherche Labellisés, 2013), to L.R., the European Research Council (ERC Consolidator Grant P-Cycles number 614244), the French Agence Nationale de la Recherche (ANR OSCI-DEEP ANR-19-NEUC-0004), and an ANITI (Artificial and Natural Intelligence Toulouse Institute) Research Chair (ANR-19-PI3A-0004) to R.V., the Studienstiftung des Deutschen Volkes (German Academic Scholarship Foundation) to B.Z., the European Union (ERC Grant Agreement n. 339490 “Cortic_al_gorithms” and grant agreements 720270 and 785907 “Human Brain Project SGA1 and SGA2’) and the Friends Foundation of the Netherlands Institute for Neuroscience to P.R.R.

Publisher Copyright:
© 2021, The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Funding

We are grateful to C.J. Stam, E. van Dellen, L. Douw, P. Ris, S. Claus, D. Velis, and R. Joosten for help with obtaining ethics approval and for technical help with the patients and recordings. This work was supported by grants from the French Agence Nationale de la Recherche (ANR-12-JSH2-0004-01 and ANR AI-REPS–18-CE37-0007-01), the Fyssen foundation, and the Université Paul Sabatier, Toulouse, France (BQR, 2009 and Appel à Projets de Recherche Labellisés, 2013), to L.R., the European Research Council (ERC Consolidator Grant P-Cycles number 614244), the French Agence Nationale de la Recherche (ANR OSCI-DEEP ANR-19-NEUC-0004), and an ANITI (Artificial and Natural Intelligence Toulouse Institute) Research Chair (ANR-19-PI3A-0004) to R.V., the Studienstiftung des Deutschen Volkes (German Academic Scholarship Foundation) to B.Z., the European Union (ERC Grant Agreement n. 339490 “Cortic_al_gorithms” and grant agreements 720270 and 785907 “Human Brain Project SGA1 and SGA2’) and the Friends Foundation of the Netherlands Institute for Neuroscience to P.R.R.

FundersFunder number
ANITI
ANR-12-JSH2-0004-0118-CE37-0007-01
Artificial and Natural Intelligence Toulouse Institute) Research ChairANR-19-PI3A-0004
Friends Foundation of the Netherlands Institute for Neuroscience
German Academic Scholarship Foundation
Université Paul Sabatier
Horizon 2020 Framework Programme339490, 785907, 720270, 614244
European Commission
European Research CouncilANR-19-NEUC-0004
Agence Nationale de la RechercheNatural Intelligence Toulouse Institute) Research Chair (ANR-19-PI3A-0004), ANR AI-REPS–18-CE37-0007-01
Fondation Fyssen
Studienstiftung des Deutschen Volkes

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