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 and Pieter R. Roelfsema
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Leila Reddy: Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier
Matthew W. Self: Netherlands Institute for Neuroscience (KNAW)
Benedikt Zoefel: Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier
Marlène Poncet: Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier
Jessy K. Possel: Netherlands Institute for Neuroscience (KNAW)
Judith C. Peters: Netherlands Institute for Neuroscience (KNAW)
Johannes C. Baayen: Amsterdam University Medical Centers, location VUmc, Departments of Neurophysiology and Neurosurgery
Sander Idema: Amsterdam University Medical Centers, location VUmc, Departments of Neurophysiology and Neurosurgery
Rufin VanRullen: Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier
Pieter R. Roelfsema: Netherlands Institute for Neuroscience (KNAW)

Nature Communications, 2021, vol. 12, issue 1, 1-9

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-25150-0

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