Dendritic Kv4.2 potassium channels selectively mediate spatial pattern separation in the dentate gyrus

Marie Oulé; Erika Atucha; Tenyse M Wells; Tamar Macharadze; Magdalena M Sauvage; Michael R Kreutz; Jeffrey Lopez-Rojas

doi:10.1016/j.isci.2021.102876

Dendritic Kv4.2 potassium channels selectively mediate spatial pattern separation in the dentate gyrus

iScience. 2021 Jul 16;24(8):102876. doi: 10.1016/j.isci.2021.102876. eCollection 2021 Aug 20.

Authors

Marie Oulé¹, Erika Atucha², Tenyse M Wells², Tamar Macharadze^{1

3}, Magdalena M Sauvage^{2

4

5}, Michael R Kreutz^{1

5

6

7}, Jeffrey Lopez-Rojas^{1

5

8}

Affiliations

¹ Research Group Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany.
² Functional Architecture of Memory Department, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany.
³ Department of Anesthesiology and Intensive Care Medicine, Otto-von-Guericke-University, 39120 Magdeburg, Germany.
⁴ Otto von Guericke University, Medical Faculty, Functional Neuroplasticity Department, 39120, Magdeburg, Germany.
⁵ Center for Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany.
⁶ Leibniz Group 'Dendritic Organelles and Synaptic Function', University Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology (ZMNH), 20251 Hamburg, Germany.
⁷ German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany.
⁸ Department of Neuroscience, The Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10027, USA.

Abstract

The capacity to distinguish comparable experiences is fundamental for the recall of similar memories and has been proposed to require pattern separation in the dentate gyrus (DG). However, the cellular mechanisms by which mature granule cells (GCs) of the DG accomplish this function are poorly characterized. Here, we show that Kv4.2 channels selectively modulate the excitability of medial dendrites of dentate GCs. These dendrites are targeted by the medial entorhinal cortex, the main source of spatial inputs to the DG. Accordingly, we found that the spatial pattern separation capability of animals lacking the Kv4.2 channel is significantly impaired. This points to the role of intrinsic excitability in supporting the mnemonic function of the dentate and to the Kv4.2 channel as a candidate substrate promoting spatial pattern separation.

Keywords: Biological sciences; Cellular neuroscience; Neuroscience.