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Intraneuronal chloride accumulation via NKCC1 is not essential for hippocampal network development in vivo

Jürgen Graf, Chuanqiang Zhang, Stephan Lawrence Marguet, Tanja Herrmann, Tom Flossmann, Robin Hinsch, Vahid Rahmati, Madlen Guenther, Christiane Frahm, Anja Urbach, Ricardo Melo Neves, Otto W. Witte, Stefan J. Kiebel, Dirk Isbrandt, Christian A. Hübner, Knut Holthoff, Knut Kirmse
doi: https://doi.org/10.1101/2020.07.13.200014
Jürgen Graf
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Chuanqiang Zhang
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
6Laboratory of Sensory Processing, Brain Mind Institute, Faculty of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), CH-1015 Lausanne, Switzerland
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Stephan Lawrence Marguet
2Institute for Molecular and Behavioral Neuroscience, University of Cologne, 50937 Cologne, Germany
3German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany
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Tanja Herrmann
4Institute of Human Genetics, Jena University Hospital, 07747Jena, Germany
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Tom Flossmann
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
7Centre for Discovery Brain Sciences, Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, United Kingdom
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Robin Hinsch
2Institute for Molecular and Behavioral Neuroscience, University of Cologne, 50937 Cologne, Germany
3German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany
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Vahid Rahmati
5Department of Psychology, Technical University Dresden, 01187 Dresden, Germany
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Madlen Guenther
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Christiane Frahm
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Anja Urbach
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Ricardo Melo Neves
2Institute for Molecular and Behavioral Neuroscience, University of Cologne, 50937 Cologne, Germany
3German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany
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Otto W. Witte
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Stefan J. Kiebel
5Department of Psychology, Technical University Dresden, 01187 Dresden, Germany
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Dirk Isbrandt
2Institute for Molecular and Behavioral Neuroscience, University of Cologne, 50937 Cologne, Germany
3German Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany
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Christian A. Hübner
4Institute of Human Genetics, Jena University Hospital, 07747Jena, Germany
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Knut Holthoff
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
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Knut Kirmse
1Hans-Berger Department of Neurology, Jena University Hospital, 07747 Jena, Germany
8Institute of Physiology, Department of Neurophysiology, University of Würzburg, 97070 Würzburg, Germany
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  • For correspondence: knut.kirmse@med.uni-jena.de
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Abstract

NKCC1 is the primary transporter mediating chloride uptake in immature principal neurons, but its role in the development of in vivo network dynamics and cognitive abilities remains unknown. Here, we address the function of NKCC1 in developing mice using electrophysiological, optical and behavioral approaches. We report that NKCC1 deletion from telencephalic glutamatergic neurons decreases in-vitro excitatory GABA actions and impairs neuronal synchrony in neonatal hippocampal brain slices. In vivo, it has a minor impact on correlated spontaneous activity in the hippocampus and does not affect network activity in the intact visual cortex. Moreover, long-term effects of the developmental NKCC1 deletion on synaptic maturation, network dynamics and behavioral performance are subtle. Our data reveal a neural network function of depolarizing GABA in the hippocampus in vivo, but challenge the hypothesis that NKCC1 is essential for major aspects of hippocampal development.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 13, 2020.
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Intraneuronal chloride accumulation via NKCC1 is not essential for hippocampal network development in vivo
Jürgen Graf, Chuanqiang Zhang, Stephan Lawrence Marguet, Tanja Herrmann, Tom Flossmann, Robin Hinsch, Vahid Rahmati, Madlen Guenther, Christiane Frahm, Anja Urbach, Ricardo Melo Neves, Otto W. Witte, Stefan J. Kiebel, Dirk Isbrandt, Christian A. Hübner, Knut Holthoff, Knut Kirmse
bioRxiv 2020.07.13.200014; doi: https://doi.org/10.1101/2020.07.13.200014
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Intraneuronal chloride accumulation via NKCC1 is not essential for hippocampal network development in vivo
Jürgen Graf, Chuanqiang Zhang, Stephan Lawrence Marguet, Tanja Herrmann, Tom Flossmann, Robin Hinsch, Vahid Rahmati, Madlen Guenther, Christiane Frahm, Anja Urbach, Ricardo Melo Neves, Otto W. Witte, Stefan J. Kiebel, Dirk Isbrandt, Christian A. Hübner, Knut Holthoff, Knut Kirmse
bioRxiv 2020.07.13.200014; doi: https://doi.org/10.1101/2020.07.13.200014

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