The medial entorhinal cortex is part of a neural system for mapping the position of an individual within a physical environment1. Grid cells, a key component of this system, fire in a characteristic hexagonal pattern of locations2, and are organized in modules3 that collectively form a population code for the animal’s allocentric position1. The invariance of the correlation structure of this population code across environments4,5 and behavioural states6,7, independent of specific sensory inputs, has pointed to intrinsic, recurrently connected continuous attractor networks (CANs) as a possible substrate of the grid pattern1,8–11. However, whether grid cell networks show continuous attractor dynamics, and how they interface with inputs from the environment, has remained unclear owing to the small samples of cells obtained so far. Here, using simultaneous recordings from many hundreds of grid cells and subsequent topological data analysis, we show that the joint activity of grid cells from an individual module resides on a toroidal manifold, as expected in a two-dimensional CAN. Positions on the torus correspond to positions of the moving animal in the environment. Individual cells are preferentially active at singular positions on the torus. Their positions are maintained between environments and from wakefulness to sleep, as predicted by CAN models for grid cells but not by alternative feedforward models12. This demonstration of network dynamics on a toroidal manifold provides a population-level visualization of CAN dynamics in grid cells.

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We introduce a novel data-driven approach to discover and decode features in the neural code coming from large population neural recordings with minimal assumptions, using cohomological feature extraction. We apply our approach to neural recordings of mice moving freely in a box, where we find a circular feature. We then observe that the decoded value corresponds well to the head direction of the mouse. Thus we capture head direction cells and decode the head direction from the neural population activity without having to process the behaviour of the mouse. Interestingly, the decoded values convey more information about the neural activity than the tracked head direction does, with differences that have some spatial organization. Finally, we note that the residual population activity, after the head direction has been accounted for, retains some low-dimensional structure which is correlated with the speed of the mouse.

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We give a new introduction to hyperstructures and higher order structures in general. A specific implementation of a hyperstructure we call Abstract Matter, and we argue that this is a suitable model for studying and simulating various kinds of both organic and inorganic matter — even cognitive matter.