Synchronous activity patterns in the dentate gyrus during immobility
- University of Bonn Medical Center, Germany
- University of Tübingen, Germany
Abstract
The hippocampal dentate gyrus is an important relay conveying sensory information from the entorhinal cortex to the hippocampus proper. During exploration, the dentate gyrus has been proposed to act as a pattern separator. However, the dentate gyrus also shows structured activity during immobility and sleep. The properties of these activity patterns at cellular resolution, and their role in hippocampal-dependent memory processes have remained unclear. Using dual-color in-vivo two-photon Ca2+ imaging, we show that in immobile mice dentate granule cells generate sparse, synchronized activity patterns associated with entorhinal cortex activation. These population events are structured and modified by changes in the environment; and they incorporate place- and speed cells. Importantly, they are more similar than expected by chance to population patterns evoked during self-motion. Using optogenetic inhibition, we show that granule cell activity is not only required during exploration, but also during immobility in order to form dentate gyrus-dependent spatial memories.
Data availability
Binarized imaging traces of all cells from all experiment sessions are available on Dryad. https://doi.org/10.5061/dryad.mkkwh70z6.
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Synchronous activity patterns in the dentate gyrus during immobilityDryad Digital Repository, doi:10.5061/dryad.mkkwh70z6.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (SFB 1089,Project C04)
- Heinz Beck
Deutsche Forschungsgemeinschaft (EXC 2064/1 PN 390727645)
- Jakob H Macke
- Heinz Beck
Alexander von Humboldt-Stiftung (PSI)
- Kurtulus Golcuk
Volkswagen Foundation
- Oliver Braganza
- Laura A Ewell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All animal experiments were conducted in accordance with European (2010/63/EU) and federal law (TierSchG, TierSchVersV) on animal care and use and approved by the county of North-Rhine Westphalia (LANUV AZ 84-02.04.2015.A524, AZ 81-02.04.2019.A216).
Copyright
© 2021, Pofahl et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Synchronous activity patterns in the dentate gyrus during immobility
eLife 10:e65786.
https://doi.org/10.7554/eLife.65786
Further reading
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- Neuroscience
Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.
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