Rebound spiking in layer II medial entorhinal cortex stellate cells: Possible mechanism of grid cell function

Christopher F. Shay, Michele Ferrante, G. William Chapman IV, Michael E. Hasselmo

Abstract:

Rebound spiking properties of medial entorhinal cortex (mEC) stellate cells induced by inhibition may
underlie their functional properties in awake behaving rats, including the temporal phase separation
of distinct grid cells and differences in grid cell firing properties. We investigated rebound spiking properties using whole cell patch recording in entorhinal slices, holding cells near spiking threshold and delivering sinusoidal inputs, superimposed with realistic inhibitory synaptic inputs to test the capacity of cells
to selectively respond to specific phases of inhibitory input. Stellate cells showed a specific phase range of
hyperpolarizing inputs that elicited spiking, but non-stellate cells did not show phase specificity. In both
cell types, the phase range of spiking output occurred between the peak and subsequent descending zero
crossing of the sinusoid. The phases of inhibitory inputs that induced spikes shifted earlier as the baseline
sinusoid frequency increased, while spiking output shifted to later phases. Increases in magnitude of the
inhibitory inputs shifted the spiking output to earlier phases. Pharmacological blockade of h-current
abolished the phase selectivity of hyperpolarizing inputs eliciting spikes. A network computational model
using cells possessing similar rebound properties as found in vitro produces spatially periodic firing properties resembling grid cell firing when a simulated animal moves along a linear track. These results suggest that the ability of mEC stellate cells to fire rebound spikes in response to a specific range of phases of
inhibition could support complex attractor dynamics that provide completion and separation to maintain
spiking activity of specific grid cell populations.