Spatiotemporally random and diverse grid cell spike patterns contribute to the transformation of grid cell to place cell in a neural network model

Abstract

The medial entorhinal cortex and the hippocampus are brain regions specialized in spatial information processing. While an animal navigates around an environment, grid cells in the medial entorhinal cortex spike at multiple discrete locations, forming hexagonal grid patterns, and each grid cell is spatiotemporally dynamic with a different grid size, spacing, and orientation. In contrast, place cells in the hippocampus spike when an animal is at one or more specific locations, called a "place field". While an animal traverses through a place field, the place cell's spike phases relative to the hippocampal theta-frequency oscillation advance in phase, known as the "spike phase precession" phenomenon and each spike encodes the specific location within the place field. Interestingly, the medial entorhinal cortical grid cells and the hippocampal place cells are only one excitatory synapse apart. However, how the spatiotemporally dynamic multi-peaked grid cell activities are transformed into hippocampal place cell activities with spike phase precession phenomenon is yet unknown. To address this question, we construct an anatomically and physiologically realistic neural network model comprised of 10,000 grid cell models, each with a spatiotemporally dynamic grid patterns and a place cell model connected by excitatory synapses. Using this neural network model, we show that grid cells' spike activities with spatiotemporally random and diverse grid orientation, spacing, and phases as inputs to place cell are able to generate a place field with spike phase precession. These results indicate that spatiotemporally random and diverse grid cell spike activities are essential for the formation of place cell activity observed in vivo.