Entorhinal cortex receptive fields are modulated by spatial attention, even without movement.

Abstract

Grid cells have been identified in the entorhinal cortex in a variety of species and allow for the precise decoding of position in space (1-7). Along with potentially playing an important role in navigation, grid cells have recently been hypothesized to make a general contribution to mental operations, including remembering the past and thinking about the future (8,9). A prerequisite for this hypothesis is that grid cell activity does not critically depend on physical movement. Directed attention, which contributes to virtually all mental operations and can be separated from physical movement provides a good test case to investigate this hypothesis. Overt attention in the form of fixational eye movements leads to grid-like firing fields in the monkey entorhinal cortex (3). Here we show that movement of covert attention, without any physical movement, also elicits spatial receptive fields with a triangular tiling of the space. In monkeys trained to maintain central fixation while covertly attending to a stimulus moving in the periphery we identified a significant population (20/141, 14% neurons at a FDR<5%) of entorhinal cells with spatially structured receptive fields. Further, we were able to identify a population of neurons that were labeled as grid cells on an individual basis. This contrast with our recordings obtained in the hippocampus, where grid-like representations were not observed. Our results provide compelling evidence that neurons in macaque entorhinal cortex do not rely on physical movement. Notably, these results support the notion that grid cells may be capable of serving a variety of different cognitive functions and suggest that grid cells are a versatile component of many neural algorithms.