4.8 Article

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

Journal

NATURE COMMUNICATIONS
Volume 12, Issue 1, Pages -

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41467-021-25150-0

Keywords

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Funding

  1. French Agence Nationale de la Recherche [ANR-12-JSH2-0004-01, ANR AI-REPS-18-CE37-0007-01, ANR OSCI-DEEP ANR-19-NEUC-0004]
  2. Fyssen foundation
  3. Universite Paul Sabatier, Toulouse, France (BQR)
  4. European Research Council [614244]
  5. ANITI (Artificial and Natural Intelligence Toulouse Institute) Research Chair [ANR-19-PI3A-0004]
  6. Studienstiftung des Deutschen Volkes (German Academic Scholarship Foundation)
  7. European Union [339490, 720270, 785907]
  8. Friends Foundation of the Netherlands Institute for Neuroscience
  9. European Research Council (ERC) [614244] Funding Source: European Research Council (ERC)
  10. Agence Nationale de la Recherche (ANR) [ANR-12-JSH2-0004] Funding Source: Agence Nationale de la Recherche (ANR)

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Research in the human temporal lobe shows that the timing of neuronal activity relative to theta brain oscillation reflects sequence order. The study found that spikes in three consecutive items in a sequence were phase-locked at distinct phases of the theta oscillation, with spikes being fired at progressively earlier phases as the sequence advanced.
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. Previous work has shown that in rodents phase precession - the phase of action potentials relative to the theta oscillation - is associated with the representation of sequential locations. Here the authors demonstrate that phase precession also occurs in the human hippocampus using single neuron and LFP recordings.

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