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
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We present near-atomic-resolution cryoEM structures of the mammalian voltage-gated potassium channel Kv1.2 in open, C-type inactivated, toxin-blocked and sodium-bound states at 3.2 Å, 2.5 Å, 3.2 Å, and 2.9 Å. These structures, all obtained at nominally zero membrane potential in detergent micelles, reveal distinct ion-occupancy patterns in the selectivity filter. The first two structures are very similar to those reported in the related Shaker channel and the much-studied Kv1.2–2.1 chimeric channel. On the other hand, two new structures show unexpected patterns of ion occupancy. First, the toxin α-Dendrotoxin, like Charybdotoxin, is seen to attach to the negatively-charged channel outer mouth, and a lysine residue penetrates into the selectivity filter, with the terminal amine coordinated by carbonyls, partially disrupting the outermost ion-binding site. In the remainder of the filter two densities of bound ions are observed, rather than three as observed with other toxin-blocked Kv channels. Second, a structure of Kv1.2 in Na+ solution does not show collapse or destabilization of the selectivity filter, but instead shows an intact selectivity filter with ion density in each binding site. We also attempted to image the C-type inactivated Kv1.2 W366F channel in Na+ solution, but the protein conformation was seen to be highly variable and only a low-resolution structure could be obtained. These findings present new insights into the stability of the selectivity filter and the mechanism of toxin block of this intensively studied, voltage-gated potassium channel.
