Andreas Herz: Depolarizing afterpotentials shape the burst activity of grid cells during navigation

LMU Munich

Grid cells in the medial entorhinal cortex (MEC) of navigating rodents encode the animal's spatial environment using lattices of hexagonally arranged firing fields. Their spike trains are organized on multiple time scales and include high-frequency bursts in the 150-300 Hz range. A mechanistic understanding of these burst sequences is, however, largely missing. We reanalyzed whole-cell recordings from male mice running in virtual corridors (Domnisoru et al., 2013) and tetrode data obtained during movements in real two-dimensional arenas (Latuske et al., 2015). The membrane potentials of some grid cells recorded in virtual reality showed depolarizing afterpotentials (DAPs) well known from in-vitro studies of MEC principal neurons. All such cells were located in Layer II, generated bursts, and their inter-spike intervals (ISIs) were typically between 5 and 15 milliseconds. The ISI distributions of all other Layer-II cells peaked sharply at ~ 4.1 milliseconds and varied only minimally across that group (standard deviation: 0.1ms). This dichotomy in burst behavior is readily explained by the cell-group-specific dynamics of spike afterpotentials. All remaining neurons were sparsely bursting and those with known location populated Layer III. A cluster analysis of the extracellular recordings led to the same groupings and showed that the two bursty cell groups recorded in the open field did not differ in their spatial coding properties. As the ion-channels underlying DAPs can be modulated in many ways, our results suggest that temporal features of grid-cell activity can be altered to serve different functions without affecting the cells' spatial tuning characteristics.

 

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