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 co

Toroidal topology of population activity in grid cells

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2022-01-12 23:30:07

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 pattern1,8,9,10,11. 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.

The idea of a CAN has become one of the most influential concepts in theoretical systems neuroscience13,14,15. A CAN is a network in which recurrent synaptic connectivity constrains the joint activity of cells to a continuous low-dimensional repertoire of possible coactivation patterns in the presence of a wide range of external inputs. Few systems are more suitable for analysis of CAN dynamics than the spatial mapping circuits of the rodent brain, owing to the continuous, low-dimensional nature of space, and the availability and interpretability of data from these circuits1,2,3,4,5,6. In medial entorhinal cortex (MEC) and surrounding areas, head direction cells16 encode orientation whereas grid cells2 encode position. CAN models conceptualize the neural representations of these variables as spanning periodic one- or two-dimensional (1D or 2D) continua on a ring17,18,19 or a torus1,8,9,10,11, respectively. In this scheme, activity within the neural network stabilizes as a localized bump when cells are ordered according to their preferred firing directions or locations in physical space. The activity bump may be smoothly translated along the network continuum by speed and direction inputs, or by external sensory cues.

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