Movement dependence and layer specificity of entorhinal phase precession in two-dimensional environments

PLoS One. 2014 Jun 24;9(6):e100638. doi: 10.1371/journal.pone.0100638. eCollection 2014.


As a rat moves, grid cells in its entorhinal cortex (EC) discharge at multiple locations of the external world, and the firing fields of each grid cell span a hexagonal lattice. For movements on linear tracks, spikes tend to occur at successively earlier phases of the theta-band filtered local field potential during the traversal of a firing field - a phenomenon termed phase precession. The complex movement patterns observed in two-dimensional (2D) open-field environments may fundamentally alter phase precession. To study this question at the behaviorally relevant single-run level, we analyzed EC spike patterns as a function of the distance traveled by the rat along each trajectory. This analysis revealed that cells across all EC layers fire spikes that phase-precess; indeed, the rate and extent of phase precession were the same, only the correlation between spike phase and path length was weaker in EC layer III. Both slope and correlation of phase precession were surprisingly similar on linear tracks and in 2D open-field environments despite strong differences in the movement statistics, including running speed. While the phase-precession slope did not correlate with the average running speed, it did depend on specific properties of the animal's path. The longer a curving path through a grid-field in a 2D environment, the shallower was the rate of phase precession, while runs that grazed a grid field tangentially led to a steeper phase-precession slope than runs through the field center. Oscillatory interference models for grid cells do not reproduce the observed phenomena.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials*
  • Algorithms
  • Animals
  • Entorhinal Cortex / physiology*
  • Models, Neurological
  • Movement*
  • Neurons / physiology*
  • Rats

Grant support

This work was supported by the Deutsche Forschungsgemeinschaft Grants SFB 618 TP B3 and GRK 1123, and the German Federal Ministry for Education and Research Grants 01GQ0440, 01GQ0901, 01GQ0972, and 01GQ1001A. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.