Grid cells in the rat entorhinal cortex display strikingly regular firing responses to the animal's position in 2-D space and have been hypothesized to form the neural substrate for dead-reckoning. However, errors accumulate rapidly when velocity inputs are integrated in existing models of grid cell activity. To produce grid-cell-like responses, these models would require frequent resets triggered by external sensory cues. Such inadequacies, shared by various models, cast doubt on the dead-reckoning potential of the grid cell system. Here we focus on the question of accurate path integration, specifically in continuous attractor models of grid cell activity. We show, in contrast to previous models, that continuous attractor models can generate regular triangular grid responses, based on inputs that encode only the rat's velocity and heading direction. We consider the role of the network boundary in the integration performance of the network and show that both periodic and aperiodic networks are capable of accurate path integration, despite important differences in their attractor manifolds. We quantify the rate at which errors in the velocity integration accumulate as a function of network size and intrinsic noise within the network. With a plausible range of parameters and the inclusion of spike variability, our model networks can accurately integrate velocity inputs over a maximum of ∼10–100 meters and ∼1–10 minutes. These findings form a proof-of-concept that continuous attractor dynamics may underlie velocity integration in the dorsolateral medial entorhinal cortex. The simulations also generate pertinent upper bounds on the accuracy of integration that may be achieved by continuous attractor dynamics in the grid cell network. We suggest experiments to test the continuous attractor model and differentiate it from models in which single cells establish their responses independently of each other.
We examine simultaneously recorded spikes from multiple grid cells, to elucidate mechanisms underlying their activity. We demonstrate that grid cell population activity, among cells with similar spatial periods, is confined to lie close to a 2-dimensional manifold: grid cells differ only along two dimensions of their responses and are otherwise nearly identical. The relationships between cell pairs are conserved despite extensive deformations of single-neuron responses. Results from novel environments suggest such structure is not inherited from hippocampal or external sensory inputs. Across conditions, cell-cell relationships are better conserved than the responses of single cells. Finally, the system is continually subject to perturbations that were the 2-d manifold not attractive, would drive the system to inhabit a different region of state-space than observed. Together, these findings have strong implications for theories of grid cell activity, and provide compelling support for the general hypothesis that the brain computes using low-dimensional continuous attractors.
We characterize the relationship between the simultaneously recorded quantities of rodent grid cell firing and the position of the rat. The formalization reveals various properties of grid cell activity when considered as a neural code for representing and updating estimates of the rat's location. We show that, although the spatially periodic response of grid cells appears wasteful, the code is fully combinatorial in capacity. The resulting range for unambiguous position representation is vastly greater than the Ϸ1-10 m periods of individual lattices, allowing for unique high-resolution position specification over the behavioral foraging ranges of rats, with excess capacity that could be used for error correction. Next, we show that the merits of the grid cell code for position representation extend well beyond capacity and include arithmetic properties that facilitate position updating. We conclude by considering the numerous implications, for downstream readouts and experimental tests, of the properties of the grid cell code.
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