Abstract

Place and grid cells in the rodent hippocampal formation tend to fire spikes at successively earlier phases relative to the local field potential theta rhythm as the animal runs through the cell's firing field on a linear track. However, this ‘phase precession’ effect is less well characterized during foraging in two-dimensional open field environments. Here, we mapped runs through the firing fields onto a unit circle to pool data from multiple runs. We asked which of seven behavioural and physiological variables show the best circular–linear correlation with the theta phase of spikes from place cells in hippocampal area CA1 and from grid cells from superficial layers of medial entorhinal cortex. The best correlate was the distance to the firing field peak projected onto the animal's current running direction. This was significantly stronger than other correlates, such as instantaneous firing rate and time-in-field, but similar in strength to correlates with other measures of distance travelled through the firing field. Phase precession was stronger in place cells than grid cells overall, and robust phase precession was seen in traversals through firing field peripheries (although somewhat less than in traversals through the centre), consistent with phase coding of displacement along the current direction. This type of phase coding, of place field distance ahead of or behind the animal, may be useful for allowing calculation of goal directions during navigation.

Highlights

  • Place cells [1] and grid cells [2] recorded in the hippocampus and medial entorhinal cortex of freely moving rodents have spatially modulated firing patterns

  • When the animal runs through the firing field of a place or grid cell, the cell typically fires short bursts of one or more action potentials (‘spikes’) whose phase relative to the local field potential (LFP) theta shifts systematically from later to earlier phases, a phenomenon known as theta phase precession [5,10]

  • We identified all of the continuous runs through a firing field, we mapped the locations of the run onto a unit circle in rstb.royalsocietypublishing.org Phil

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Summary

Introduction

Place cells [1] and grid cells [2] recorded in the hippocampus and medial entorhinal cortex of freely moving rodents have spatially modulated firing patterns. (In larger environments, place cells have multiple fields, but the fields lack periodicity [3], see [4].) In addition to their spatially modulated firing rates, place cells [5] and grid cells (at least those in layer II [6]) show a form of temporal or phase coding relative to the ongoing theta rhythm of the local field potential (LFP). The spikes are fired at the peaks of a theta-band membrane potential oscillation which shows phase precession relative to the LFP, in both place [11] and grid cells [12,13].

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