Dentate granule cells in the rat hippocampal formation have the behavioral characteristics of theta neurons.

Recordings were made from the dentate gyrus granule cell layer of freely-moving rats. The neurons recorded from the layer were divisible into 3 classes using a combination of electrophysiological and behavioral criteria; the duration of the extracellularly recorded unfiltered action potential provided the most reliable means of differentiating between cell types. Class I and class II neurons always fired in short duration single action potentials, while class III neurons had broader waveforms and occasionally were observed to fire complex spikes. As the most obvious behavioral correlate of class I and class II neurons was movement of the rat, these cells correspond to the theta cells of Ranck. Class III neurons for which a behavioral correlate was observed had the characteristics of the place cells described by O'Keefe. The neurons of classes I and II comprised 89% (56 of 63) of the total population sampled in the granule cell layer. Most of these neurons (49 of 56) discharged at short latency in response to a stimulus delivered via the perforant pathway; in contrast, none of the class III neurons observed were activated in this way. Horseradish peroxidase or Fast Green dye ejection through glass microelectrodes recording class I cell activity in urethane-anesthetized animals revealed the electrode tip to be in the granule cell layer in 27 of 27 cases. Six single class I neurons were also antidromically activated by a stimulus from an electrode placed in the hippocampal mossy fibers, and collision testing was successful in all cases. It is concluded that the dentate granule cells are theta cells.