Retuning of hippocampal representations during sleep

Kourosh Maboudi, Bapun Giri, Hiroyuki Miyawaki, Caleb Kemere and Kamran Diba ()
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Kourosh Maboudi: University of Michigan Medical School
Bapun Giri: University of Michigan Medical School
Hiroyuki Miyawaki: University of Wisconsin-Milwaukee
Caleb Kemere: Rice University
Kamran Diba: University of Michigan Medical School

Nature, 2024, vol. 629, issue 8012, 630-638

Abstract: Abstract Hippocampal representations that underlie spatial memory undergo continuous refinement following formation1. Here, to track the spatial tuning of neurons dynamically during offline states, we used a new Bayesian learning approach based on the spike-triggered average decoded position in ensemble recordings from freely moving rats. Measuring these tunings, we found spatial representations within hippocampal sharp-wave ripples that were stable for hours during sleep and were strongly aligned with place fields initially observed during maze exploration. These representations were explained by a combination of factors that included preconfigured structure before maze exposure and representations that emerged during θ-oscillations and awake sharp-wave ripples while on the maze, revealing the contribution of these events in forming ensembles. Strikingly, the ripple representations during sleep predicted the future place fields of neurons during re-exposure to the maze, even when those fields deviated from previous place preferences. By contrast, we observed tunings with poor alignment to maze place fields during sleep and rest before maze exposure and in the later stages of sleep. In sum, the new decoding approach allowed us to infer and characterize the stability and retuning of place fields during offline periods, revealing the rapid emergence of representations following new exploration and the role of sleep in the representational dynamics of the hippocampus.

Date: 2024
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DOI: 10.1038/s41586-024-07397-x

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