Grid cells without theta oscillations in the entorhinal cortex of bats

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 environment. Although grid cells have been characterized in detail in rats, 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 dynamics, 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 grid. So far, these models could not be dissociated experimentally, because rodent grid cells always co-exist with continuous theta oscillations. Here we used a novel animal model, the Egyptian fruit bat, 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 oscillations, 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.

Saccade direction encoding in the primate entorhinal cortex during visual exploration

“…S3). This tuning correlation is similar to the anatomical gradient observed in grid cell spacing (1,6,15) and is consistent with the recently described increase in the tuning width of head-direction cells along the dorsoventral axis in rodents (16). Thus, colocalized visual grid cells and SD cells demonstrate similar anatomical gradients with respect to the scale of the spatial representation.…”

From chemotaxis to the cognitive map: The function of olfaction

“…As with fruit-eating simians, these bats forage for a food resource that can be tracked in space and time. Cognitive mapping has also been demonstrated in a wild megabat, the Egyptian fruit bat (51), as have medial entorhinal grid cells (52). Concordant with this proposed predictor status, megabats show an intermediate LI/intermediate IS pattern (3).…”

Grid cells and cortical representation

“…Place cells and grid cells were discovered in rats but similar cells have subsequently been reported in mice [13][14][15] , bats 16,17 , monkeys [18][19][20][21] , and humans 22,23 , although the bulk of work on entorhinal-hippocampal spatial representation is still performed in rodents. The strong correspondence in each species between entorhinal-hippocampal firing patterns and a measurable property of the external world -the location of the animal -makes the spatial representation circuit a powerful experimental model system for understanding neural computation at the highest levels of the association cortices, many synapses away from sensory receptors and motor outputs.…”