A Novel Mechanism for the Grid-to-Place Cell Transformation Revealed by Transgenic Depolarization of Medial Entorhinal Cortex Layer II

Benjamin R Kanter; Christine M Lykken; Daniel Avesar; Aldis Weible; Jasmine Dickinson; Benjamin Dunn; Nils Z Borgesius; Yasser Roudi; Clifford G Kentros

doi:10.1016/j.neuron.2017.03.001

A Novel Mechanism for the Grid-to-Place Cell Transformation Revealed by Transgenic Depolarization of Medial Entorhinal Cortex Layer II

Neuron. 2017 Mar 22;93(6):1480-1492.e6. doi: 10.1016/j.neuron.2017.03.001.

Authors

Benjamin R Kanter¹, Christine M Lykken¹, Daniel Avesar², Aldis Weible², Jasmine Dickinson², Benjamin Dunn³, Nils Z Borgesius³, Yasser Roudi³, Clifford G Kentros⁴

Affiliations

¹ Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres gate 9, 7030 Trondheim, Norway; Institute of Neuroscience, University of Oregon, 1254 University of Oregon, Eugene, OR 97403, USA.
² Institute of Neuroscience, University of Oregon, 1254 University of Oregon, Eugene, OR 97403, USA.
³ Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres gate 9, 7030 Trondheim, Norway.
⁴ Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres gate 9, 7030 Trondheim, Norway; Institute of Neuroscience, University of Oregon, 1254 University of Oregon, Eugene, OR 97403, USA. Electronic address: clifford.kentros@ntnu.no.

PMID: 28334610
DOI: 10.1016/j.neuron.2017.03.001

Abstract

The spatial receptive fields of neurons in medial entorhinal cortex layer II (MECII) and in the hippocampus suggest general and environment-specific maps of space, respectively. However, the relationship between these receptive fields remains unclear. We reversibly manipulated the activity of MECII neurons via chemogenetic receptors and compared the changes in downstream hippocampal place cells to those of neurons in MEC. Depolarization of MECII impaired spatial memory and elicited drastic changes in CA1 place cells in a familiar environment, similar to those seen during remapping between distinct environments, while hyperpolarization did not. In contrast, both manipulations altered the firing rate of MEC neurons without changing their firing locations. Interestingly, only depolarization caused significant changes in the relative firing rates of individual grid fields, reconfiguring the spatial input from MEC. This suggests a novel mechanism of hippocampal remapping whereby rate changes in MEC neurons lead to locational changes of hippocampal place fields.

Keywords: chemogenetic; grid cells; hippocampus; medial entorhinal cortex; place cells; remapping; spatial memory; transgenic.

MeSH terms

Action Potentials / physiology
Animals
CA1 Region, Hippocampal / physiology*
Entorhinal Cortex / physiology*
Female
Grid Cells / physiology*
Male
Maze Learning / physiology
Mice
Mice, Transgenic
Neural Inhibition / physiology
Neurons / physiology
Place Cells / physiology*
Space Perception / physiology
Spatial Memory / physiology

Grants and funding

R01 MH097130/MH/NIMH NIH HHS/United States