Computation by oscillations: Implications of experimental data for theoretical models of grid cells

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Abstract
Recordings in awake, behaving animals demonstrate that cells in medial entorhinal cortex (mEC) show “grid cell” firing activity when a rat explores an open environment. Intracellular recording in slices from different positions along the dorsal to ventral axis show differences in intrinsic properties such as subthreshold membrane potential oscillations (MPO), resonant frequency, and the presence of the hyperpolarization‐activated cation current (h‐current). The differences in intrinsic properties correlate with differences in grid cell spatial scale along the dorsal–ventral axis of mEC. Two sets of computational models have been proposed to explain the grid cell firing phenomena: oscillatory interference models and attractor‐dynamic models. Both types of computational models are briefly reviewed, and cellular experimental evidence is interpreted and presented in the context of both models. The oscillatory interference model has variations that include an additive model and a multiplicative model. Experimental data on the voltage‐dependence of oscillations presented here support the additive model. The additive model also simulates data from ventral neurons showing large spacing between grid firing fields within the limits of observed MPO frequencies. The interactions of h‐current with synaptic modification suggest that the difference in intrinsic properties could also contribute to differences in grid cell properties due to attractor dynamics along the dorsal to ventral axis of mEC. Mechanisms of oscillatory interference and attractor dynamics may make complementary contributions to the properties of grid cell firing in entorhinal cortex.