Grid Cell Spatial Periodicity: Necessary Intercellular Interactions during Development and Behavioral Function
Final Report Abstract
Most mammals depend on their ability to navigate in order to fulfill their needs like finding food and returning to the relative safety of their home base after an exploratory journey. This ability to navigate depends on interconnected brain areas containing neurons encoding information about our location and orientation. Out of these brain regions, the medial entorhinal cortex (MEC) is the one with the most diverse population of spatially selective neurons. To gain insight into how the MEC contributes to navigation, this research project studied the activity patterns of spatially selective neurons in the MEC during exploratory behavior. In a first experiment, we discovered that excitatory neurons of the MEC can be divided into two populations base on their propensity to fire bursts of action potentials at the millisecond timescale. Bursty and non-bursty neurons differed not only in their action potentials waveforms, but also in the type of spatial information they encoded and in their interactions with high firing rate interneurons. A second study aimed at investigating how visual landmarks contribute to the spatial selectivity of grid cells of the MEC. A grid cell is a neuron that fires at several locations in an environment, and these locations of high activity are organized as a periodic grid of equilateral triangles. One major finding was that the spatial firing patterns of grid cells strongly depends on the presence of visual landmarks. When visual landmarks were absent, the spatial selectivity and periodicity of grid cells were severely reduced. This finding led us to reconsider how quickly error accumulates in our internal estimation of position when visual landmarks are absent. In a third study, we focused our efforts on the head-direction cells of the MEC. Head-direction cells are neurons that fire only when the head of an animal is oriented in a specific direction. These neurons are often considered to work like a compass, with different head-direction cells active in different directions. A key aspect of current computational models of head-direction cells is that the difference in the preferred direction of two head-direction cells should remain constant at any time. We challenged this assumption by recording head-direction cells in the MEC while manipulating the visual landmarks surrounding an animal. Surprisingly, we found that the activity of a sub-population of head-direction cells was strongly affected by manipulations of visual landmarks. Importantly, and in sharp contrast with the predictions of current computational models of head-direction cells, we found that the difference in the preferred direction of head-direction cells in this sub-population could be reshaped by the visual landmarks surrounding the animal. This implies that the mechanisms responsible for the directional firing in this sub-population of head-direction cells are fundamentally different from those at play in “classical” head-direction cells.
Publications
- (2015). Interneuron control of hippocampal oscillations. Current opinion in neurobiology, 31, 81-87
Allen K, Monyer H
(See online at https://doi.org/10.1016/j.conb.2014.08.016) - (2015). Interspike Intervals Reveal Functionally Distinct Cell Populations in the Medial Entorhinal Cortex. Journal of Neuroscience, 35, 10963-10976
Latuske P, Toader O, Allen K
(See online at https://doi.org/10.1523/JNEUROSCI.0276-15.2015) - (2016). Consolidation of recently formed hippocampal cell assembly patterns requires off-line reactivation during sharp-wave/ripples. Neuron, 92, 968-974
Van de Ven GM, Trouche S, McNamara CG, Allen K, Dupret D
(See online at https://doi.org/10.1016/j.neuron.2016.10.020) - (2016). Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex. eLife, 5, e16937
Pérez-Escobar JA, Kornienko O, Latuske P, Kohler L, Allen K
(See online at https://doi.org/10.7554/eLife.16937) - (2018). CKAMP44 modulates integration of visual inputs in the lateral geniculate nucleus. Nature Communication, 9, 261
Chen X, Aslam M, Gollisch T, Allen K, von Engelhardt J
(See online at https://doi.org/10.1038/s41467-017-02415-1) - (2018). Hippocampal remapping and its entorhinal origin. Frontiers in Behavioral Neuroscience, 11, 253
Latuske P, Kornienko O, Kohler L, Allen K
(See online at https://doi.org/10.3389/fnbeh.2017.00253) - (2018). Impaired path integration in mice with disrupted grid cell firing. Nature Neuroscience, 21, 81-91
Gil M, Ancau M, Schlesiger MI, Neitz A, Allen K, De Marco RJ, Monyer H
(See online at https://doi.org/10.1038/s41593-017-0039-3) - (2018). Non-rhythmic head-direction cells in the parahippocampal region are not constrained by attractor network dynamics. eLife, 7, e35949
Kornienko O, Latuske P, Bassler M, Kohler L, Allen K
(See online at https://doi.org/10.7554/eLife.35949)
