Grid cells without theta oscillations in the entorhinal cortex of bats

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Abstract

Grid cells provide a neural representation of space, by discharging when an animal traverses through the vertices of a periodic hexagonal grid spanning the environment1. Although grid cells have been characterized in detail in rats1,2,3,4,5,6, the fundamental question of what neural dynamics give rise to the grid structure remains unresolved. Two competing classes of models were proposed: network models, based on attractor dynamics7,8,9, and oscillatory interference models, which propose that interference between somatic and dendritic theta-band oscillations (4–10 Hz) in single neurons transforms a temporal oscillation into a spatially periodic grid10,11,12,13. So far, these models could not be dissociated experimentally, because rodent grid cells always co-exist with continuous theta oscillations4,5,6,14. Here we used a novel animal model, the Egyptian fruit bat15,16, to refute the proposed causal link between grids and theta oscillations. On the basis of our previous finding from bat hippocampus, of spatially tuned place cells in the absence of continuous theta oscillations17, we hypothesized that grid cells in bat medial entorhinal cortex might also exist without theta oscillations. Indeed, we found grid cells in bat medial entorhinal cortex that shared remarkable similarities to rodent grid cells. Notably, the grids existed in the absence of continuous theta-band oscillations, and with almost no theta modulation of grid-cell spiking—both of which are essential prerequisites of the oscillatory interference models. Our results provide a direct demonstration of grid cells in a non-rodent species. Furthermore, they strongly argue against a major class of computational models of grid cells.

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Figure 1: Bat CA1 recordings demonstrate place cells but no continuous theta oscillations.
Figure 2: Anatomical delineation of MEC in Egyptian fruit bats, and targeting of grid cells.
Figure 3: Grid-cell properties in the bat resemble those in the rat.
Figure 4: No continuous theta oscillations in bat MEC.

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Acknowledgements

We thank D. Derdikman, S. Romani, M. Ahrens and Y. Cohen for comments on the manuscript, M. Melcón for initial assistance with hippocampal CA1 recordings, M. Weinberg for veterinary oversight, and R. Eilam and C. Ra'anan for histology. This study was supported by research grants from the Israel Science Foundation and Minerva Foundation to N.U., by a Lev-Zion predoctoral excellence fellowship to M.M.Y., as well as by grants from the Norwegian Research Council and the Kavli Foundation to M.P.W.

Author information

M.M.Y. and N.U. designed the study, conducted the experiments, analysed the data and wrote the manuscript. M.P.W. performed immunohistochemical analyses, delineated the anatomical structures in the hippocampus and entorhinal cortex of Egyptian fruit bats, and verified recording sites. All authors discussed the results and commented on the manuscript.

Correspondence to Nachum Ulanovsky.

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The authors declare no competing financial interests.

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The file contains Supplementary Figures 1-22 with legends, Supplementary Methods, Supplementary Text and Data and additional references. (PDF 18634 kb)

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Yartsev, M., Witter, M. & Ulanovsky, N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103–107 (2011) doi:10.1038/nature10583

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