Differential ripple propagation along the hippocampal longitudinal axis

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Abstract

Hippocampal ripples are highly synchronous neural events critical for memory consolidation and retrieval. A minority of strong ripples has been shown to be of particular importance in situations of increased memory demands. The propagation dynamics of strong ripples inside the hippocampal formation are, however, still opaque. We analyzed ripple propagation within the hippocampal formation in a large open access dataset comprising 267 Neuropixel recordings in 49 awake, head-fixed mice. Surprisingly, strong ripples (top 10% in ripple strength) propagate differentially depending on their generation point along the hippocampal longitudinal axis. The septal hippocampal pole is able to generate longer ripples that engage more neurons and elicit spiking activity for an extended time even at considerable distances. Accordingly, a substantial portion of the variance in strong ripple duration (R² = 0.463) is explained by the ripple generation location on the longitudinal axis, in agreement with a possible distinctive role of the hippocampal septal pole in conditions of high memory demand. Moreover, we observed that the location of the ripple generation has a significant impact on the spiking rate modulation of different hippocampal subfields, even before the onset of the ripple. This finding suggests that ripple generation location plays a crucial role in shaping the neural activity across the hippocampus.

Data availability

All the code used to process the dataset is available at https://github.com/RobertoDF/De-Filippo-et-al-2022, pre-computed data structures can be downloaded at 10.6084/m9.figshare.20209913. All figures and text can be reproduced using code present in this repository, each number present in the text is directly linked to a python data structure. The original dataset is provided by the Allen Institute and available at https://allensdk.readthedocs.io/en/latest/visual_coding_neuropixels.html.

The following previously published data sets were used

1. Siegle JH
2. Jia X
3. Durand S
4. et al
(2021) Visual Coding - Neuropixels
https://knowledge.brain-map.org/data/4YYLRZZGK82FQ85NIH8/summary.

https://doi.org/10.1038/s41586-020-03171-x

Article and author information

Author details

Roberto de Filippo

Neuroscience Research Center, Charité Universitätsmedizin Berlin, Berlin, Germany

For correspondence
roberto.de-filippo@charite.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4085-9114
Dietmar Schmitz

Neuroscience Research Center, Charité Universitätsmedizin Berlin, Berlin, Germany

For correspondence
dschmitz-office@charite.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2741-5241

Funding

Deutsche Forschungsgemeinschaft (184695641 - SFB 958)

Dietmar Schmitz

Deutsche Forschungsgemeinschaft (327654276 - SFB 1315)

Dietmar Schmitz

European Research Council (810580)

Roberto de Filippo

NeuroCure Exzellenzcluster (Exc-2049-390688087)

Dietmar Schmitz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

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.