The place cell activity in three-dimensional space generated by multiple grid cell inputs

How the brain encodes spatial information is an important topic. Experimental and theoretical progresses achieved in this area mainly focused on the neuronal response in the lower-dimensional space such as a linear track or a horizontal flat arena. How the real three-dimensional (3-D) space is represented in the brain is unknown. Grid cells in the medial entorhinal cortex and the place cells in the hippocampus are the principal spatial neurons, and the grid cells provide important inputs to the place cells. In order to simulate the place cell activity in higher dimension, we proposed a rotating-integration model to generate the place field on non-horizontal surfaces for crawling animal in 3-D space. By referring to the gravity signal as an anchor, preferred directions of the grid cell will be rotated with the animal’s body plane during navigating on the surfaces. Then, multiple grid cell patterns with distributed orientations and wavelengths are integrated to form the firing field(s) of a place cell. The results can not only account for the known experimental recordings but also predict a segment planar encoding property of place cell on novel complex surfaces. It suggests that the spatial cognition for crawling animal is achieved by a mosaic of lower-dimensional codes rather than the full volumetric perception. This work can help us understand how the spatial information provided by the external physical world is represented and processed by the neuronal systems.