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

Leila Reddy (1, 2) , Matthew Self , Benedikt Zoefel (1) , Marlène Poncet (1) , Jessy Possel (3) , Judith Peters (3, 4) , Johannes Baayen (5, 6) , Sander Idema (5, 6) , Rufin Vanrullen (1, 2) , Pieter Roelfsema (3, 7, 8)

1 CERCO - Centre de recherche cerveau et cognition
2 ANITI - Artificial and Natural Intelligence Toulouse Institute
3 NIN - Netherlands Institute for Neuroscience
4 Maastricht University [Maastricht]
5 Amsterdam UMC - Amsterdam University Medical Center
6 VU University Medical Center [Amsterdam]
7 VU - Vrije Universiteit Amsterdam [Amsterdam]
8 AMC - Academic Medical Center - Academisch Medisch Centrum [Amsterdam]

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.

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 25 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 30 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.

Domaines: Sciences du Vivant [q-bio]

Leila Reddy, Matthew Self, Benedikt Zoefel, Marlène Poncet, Jessy Possel, et al.. Theta-phase dependent neuronal coding during sequence learning in human single neurons. Nature Communications, 2021, ⟨10.1101/630095⟩. ⟨hal-03001277⟩