A developmental increase of inhibition promotes the emergence of hippocampal ripples.

Mice; Animals; Interneurons/physiology; Hippocampus/physiology; Pyramidal Cells/physiology; Hippocampus; Interneurons; Pyramidal Cells; Chemistry (all); Biochemistry, Genetics and Molecular Biology (all); Multidisciplinary; Physics and Astronomy (all)

Abstract :

[en] Sharp wave-ripples (SPW-Rs) are a hippocampal network phenomenon critical for memory consolidation and planning. SPW-Rs have been extensively studied in the adult brain, yet their developmental trajectory is poorly understood. While SPWs have been recorded in rodents shortly after birth, the time point and mechanisms of ripple emergence are still unclear. Here, we combine in vivo electrophysiology with optogenetics and chemogenetics in 4 to 12-day-old mice to address this knowledge gap. We show that ripples are robustly detected and induced by light stimulation of channelrhodopsin-2-transfected CA1 pyramidal neurons only from postnatal day 10 onwards. Leveraging a spiking neural network model, we mechanistically link the maturation of inhibition and ripple emergence. We corroborate these findings by reducing ripple rate upon chemogenetic silencing of CA1 interneurons. Finally, we show that early SPW-Rs elicit a more robust prefrontal cortex response than SPWs lacking ripples. Thus, development of inhibition promotes ripples emergence.

Disciplines :

Life sciences: Multidisciplinary, general & others

Author, co-author :

Pochinok, Irina ; Institute of Developmental Neurophysiology, Center for Molecular Neurobiology (ZMNH), Hamburg Center of Neuroscience (HCNS), University Medical Center Hamburg-Eppendorf, 20251, Hamburg, Germany

Stöber, Tristan M ; Frankfurt Institute for Advanced Studies, 60438, Frankfurt am Main, Germany

Triesch, Jochen ; Frankfurt Institute for Advanced Studies, 60438, Frankfurt am Main, Germany

Chini, Mattia ^✱; Institute of Developmental Neurophysiology, Center for Molecular Neurobiology (ZMNH), Hamburg Center of Neuroscience (HCNS), University Medical Center Hamburg-Eppendorf, 20251, Hamburg, Germany. mattia.chini@zmnh.uni-hamburg.de

Hanganu-Opatz, Ileana L ^✱; Institute of Developmental Neurophysiology, Center for Molecular Neurobiology (ZMNH), Hamburg Center of Neuroscience (HCNS), University Medical Center Hamburg-Eppendorf, 20251, Hamburg, Germany. hangop@zmnh.uni-hamburg.de

^✱ These authors have contributed equally to this work.

Language :

English

Title :

A developmental increase of inhibition promotes the emergence of hippocampal ripples.

Publication date :

25 January 2024

Journal title :

Nature Communications

eISSN :

2041-1723

Publisher :

Nature Research, England

Volume :

Issue :

Pages :

738

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.nature.com/articles/s41467-024-44983-z.pdf

Funders :

DFG - Deutsche Forschungsgemeinschaft
EU - European Union

Funding text :

We thank A. Dahlmann and P. Putthoff for excellent technical assistance as well as Drs. Lingzhen Song, Xiaxia Xu, Sebastian Bitzenhofer, Johanna Kostka, Jastyn P\u00F6pplau, and Jan Marker for valuable discussions. This work was funded by grants from the German Research Foundation (Ha4466/11-1, Ha4466/20-1 and SFB 936 B5 to I.L.H.-O.), European Research Council (ERC-2015-CoG 681577 to I.L.H.-O.), Horizon 2020 MSCA-ITN (860563 to I.L. H.-O.), DEEPER (101016787 to I.L.H.-O.), Landesforschungsf\u00F6rderung Hamburg (LFF73 and LFF76 to I.L. H.-O.), the LOEWE CePTER \u2013 Center for Personalized Translational Epilepsy Research (to T.M.S.) and Johanna Quandt Foundation (to J.T.).

Available on ORBi :

since 18 March 2026

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