Phase coding by grid cells in unconstrained environments: two-dimensional phase precession

Eur J Neurosci. 2013 Aug;38(4):2526-41. doi: 10.1111/ejn.12256. Epub 2013 May 29.


Action potential timing is thought to play a critical role in neural representation. For example, theta phase precession is a robust phenomenon exhibited by spatial cells of the rat entorhinal-hippocampal circuit. In phase precession, the time a neuron fires relative to the phase of theta rhythm (6-10 Hz) oscillations in the local field potential reduces uncertainty about the position of the animal. This relationship between neural firing and behavior has made precession an important constraint for hypothetical mechanisms of temporal coding. However, challenges exist in identifying what regulates the spike timing of these cells. We have developed novel analytical techniques for mapping between behavior and neural firing that provide sufficient sensitivity to examine features of grid cell phase coding in open environments. Here, we show robust, omnidirectional phase precession by entorhinal grid cells in openfield enclosures. We present evidence that full phase precession persists regardless of how close the animal comes to the center of a firing field. Many conjunctive grid cells, previously thought to be phase locked, also exhibited phase coding. However, we were unable to detect directional- or field-specific phase coding predicted by some variants of models. Finally, we present data that suggest bursting of layer II grid cells contributes to the bimodality of phase precession. We discuss implications of these observations for models of temporal coding and propose the utility of these techniques in other domains where behavior is aligned to neural spiking.

Keywords: medial entorhinal cortex; oscillatory interference; rat; spatial navigation; theta.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Behavior, Animal / physiology
  • Data Interpretation, Statistical
  • Entorhinal Cortex / physiology*
  • Male
  • Neurons / physiology*
  • Rats
  • Rats, Long-Evans
  • Theta Rhythm