Place fields of single spikes in hippocampus involve Kcnq3 channel-dependent entrainment of complex spike bursts

Xiaojie Gao, Franziska Bender, Heun Soh, Changwan Chen, Mahsa Altafi, Sebastian Schütze, Matthias Heidenreich, Maria Gorbati, Mihaela-Anca Corbu, Marta Carus-Cadavieco, Tatiana Korotkova, Anastasios V. Tzingounis, Thomas J. Jentsch () and Alexey Ponomarenko ()
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Xiaojie Gao: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Franziska Bender: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Heun Soh: University of Connecticut
Changwan Chen: Max Planck Institute for Metabolism Research
Mahsa Altafi: Friedrich-Alexander-Universität Erlangen-Nürnberg
Sebastian Schütze: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Matthias Heidenreich: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Maria Gorbati: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Mihaela-Anca Corbu: Max Planck Institute for Metabolism Research
Marta Carus-Cadavieco: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Tatiana Korotkova: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Anastasios V. Tzingounis: University of Connecticut
Thomas J. Jentsch: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
Alexey Ponomarenko: Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract Hippocampal pyramidal cells encode an animal’s location by single action potentials and complex spike bursts. These elementary signals are believed to play distinct roles in memory consolidation. The timing of single spikes and bursts is determined by intrinsic excitability and theta oscillations (5–10 Hz). Yet contributions of these dynamics to place fields remain elusive due to the lack of methods for specific modification of burst discharge. In mice lacking Kcnq3-containing M-type K+ channels, we find that pyramidal cell bursts are less coordinated by the theta rhythm than in controls during spatial navigation, but not alert immobility. Less modulated bursts are followed by an intact post-burst pause of single spike firing, resulting in a temporal discoordination of network oscillatory and intrinsic excitability. Place fields of single spikes in one- and two-dimensional environments are smaller in the mutant. Optogenetic manipulations of upstream signals reveal that neither medial septal GABA-ergic nor cholinergic inputs alone, but rather their joint activity, is required for entrainment of bursts. Our results suggest that altered representations by bursts and single spikes may contribute to deficits underlying cognitive disabilities associated with KCNQ3-mutations in humans.

Date: 2021
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DOI: 10.1038/s41467-021-24805-2

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