How reduction of theta rhythm by medial septum inactivation may covary with disruption of entorhinal grid cell responses due to reduced cholinergic transmission
Open Access
- 1 January 2013
- journal article
- Published by Frontiers Media SA in Frontiers in Neural Circuits
- Vol. 7, 173
- https://doi.org/10.3389/fncir.2013.00173
Abstract
Oscillations in the coordinated firing of brain neurons have been proposed to play important roles in perception, cognition, attention, learning, navigation, and sensory-motor control. The network theta rhythm has been associated with properties of spatial navigation, as has the firing of entorhinal grid cells and hippocampal place cells. Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells. These results, along with properties of intrinsic membrane potential oscillations (MPOs) in slice preparations of medial entorhinal cortex (MEC), have been interpreted to support oscillatory interference models of grid cell firing. The current article shows that an alternative self-organizing map (SOM) model of grid cells can explain these data about intrinsic and network oscillations without invoking oscillatory interference. In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K+) and slow and medium after-hyperpolarization (sAHP and mAHP) channels. This alternative model can also explain data that are problematic for oscillatory interference models, including how knockout of the HCN1 gene in mice, which flattens the dorsoventral gradient in MPO frequency and resonance frequency, does not affect the development of the grid cell dorsoventral gradient of spatial scales, and how hexagonal grid firing fields in bats can occur even in the absence of theta band modulation. These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.Keywords
This publication has 61 references indexed in Scilit:
- Membrane potential dynamics of grid cellsNature, 2013
- Recurrent inhibitory circuitry as a mechanism for grid formationNature Neuroscience, 2013
- Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional TuningScience, 2011
- Accurate Path Integration in Continuous Attractor Network Models of Grid CellsPLoS Computational Biology, 2009
- Progressive increase in grid scale from dorsal to ventral medial entorhinal cortexHippocampus, 2008
- Conversion of a phase‐ to a rate‐coded position signal by a three‐stage model of theta cells, grid cells, and place cellsHippocampus, 2008
- Transient 23–30 Hz oscillations in mouse hippocampus during exploration of novel environmentsHippocampus, 2008
- An oscillatory interference model of grid cell firingHippocampus, 2007
- A Spin Glass Model of Path Integration in Rat Medial Entorhinal CortexJournal of Neuroscience, 2006
- Changes in cortical acetylcholine output induced by modulation of the nucleus basalisBrain Research Bulletin, 1986