Gao, Xiaojie, Bender, Franziska, Soh, Heun, Chen, Changwan, Altafi, Mahsa, Schuetze, Sebastian, Heidenreich, Matthias, Gorbati, Maria, Corbu, Mihaela-Anca, Carus-Cadavieco, Marta, Korotkova, Tatiana, Tzingounis, Anastasios, V, Jentsch, Thomas J. and Ponomarenko, Alexey (2021). Place fields of single spikes in hippocampus involve Kcnq3 channel-dependent entrainment of complex spike bursts. Nat. Commun., 12 (1). BERLIN: NATURE PORTFOLIO. ISSN 2041-1723

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Abstract

Hippocampal pyramidal cells encode an animal's location by single action potentials and complex spike bursts. The authors show that Kcnq3-containing M-channels synergistically with GABAergic inputs coordinate complex spike bursts during theta oscillations, which is a key mechanism for spatial coding by single spikes. 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.

Item Type: Journal Article
Creators:
CreatorsEmailORCIDORCID Put Code
Gao, XiaojieUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Bender, FranziskaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Soh, HeunUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Chen, ChangwanUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Altafi, MahsaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Schuetze, SebastianUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Heidenreich, MatthiasUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Gorbati, MariaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Corbu, Mihaela-AncaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Carus-Cadavieco, MartaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Korotkova, TatianaUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Tzingounis, Anastasios, VUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Jentsch, Thomas J.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Ponomarenko, AlexeyUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
URN: urn:nbn:de:hbz:38-597508
DOI: 10.1038/s41467-021-24805-2
Journal or Publication Title: Nat. Commun.
Volume: 12
Number: 1
Date: 2021
Publisher: NATURE PORTFOLIO
Place of Publication: BERLIN
ISSN: 2041-1723
Language: English
Faculty: Unspecified
Divisions: Unspecified
Subjects: no entry
Uncontrolled Keywords:
KeywordsLanguage
PERSISTENT NA+ CURRENT; POTASSIUM CHANNEL; ACETYLCHOLINE-RELEASE; PYRAMIDAL CELLS; THETA-RHYTHM; CHOLINERGIC SUPPRESSION; SYNAPTIC-TRANSMISSION; RAT HIPPOCAMPUS; SPATIAL MAP; K+ CURRENTMultiple languages
Multidisciplinary SciencesMultiple languages
URI: http://kups.ub.uni-koeln.de/id/eprint/59750

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