The role of oscillations in grid cells' toroidal topology (2501.19262v1)

Abstract: Persistent homology applied to the activity of grid cells in the Medial Entorhinal Cortex suggests that this activity lies on a toroidal manifold. By analyzing real data and a simple model, we show that neural oscillations play a key role in the appearance of this toroidal topology. To quantitatively monitor how changes in spike trains influence the topology of the data, we first define a robust measure for the degree of toroidality of a dataset. Using this measure, we find that small perturbations ($\sim$ 100 ms) of spike times have little influence on both the toroidality and the hexagonality of the ratemaps. Jittering spikes by $\sim$ 100-500 ms, however, destroys the toroidal topology, while still having little impact on grid scores. These critical jittering time scales fall in the range of the periods of oscillations between the theta and eta bands. We thus hypothesized that these oscillatory modulations of neuronal spiking play a key role in the appearance and robustness of toroidal topology and the hexagonal spatial selectivity is not sufficient. We confirmed this hypothesis using a simple model for the activity of grid cells, consisting of an ensemble of independent rate-modulated Poisson processes. When these rates were modulated by oscillations, the network behaved similarly to the real data in exhibiting toroidal topology, even when the position of the fields were perturbed. In the absence of oscillations, this similarity was substantially lower. Furthermore, we find that the experimentally recorded spike trains indeed exhibit temporal modulations at the eta and theta bands, and that the ratio of the power in the eta band to that of the theta band, $A_{\eta}/A_{\theta}$, correlates with the critical jittering time at which the toroidal topology disappears.