The behavior of mossy cells of the rat dentate gyrus during theta oscillations in vivo.

Intracellular current clamp recordings were obtained from mossy cells (n = 6, identified by intracellular injection of biocytin) of the dorsal dentate gyrus from rats under ketamine-xylazine anesthesia. During electroencephalographic theta rhythm (4-6 Hz), recorded with a macroelectrode placed in the contralateral dorsal hippocampus near the fissure, mossy cells displayed intracellular membrane potential oscillations at low frequencies (4-6 Hz) which appeared to be phase locked to the electroencephalographic theta rhythm. The frequency of the intracellular theta rhythm was independent of the membrane potential. However, the phase difference between the intracellular and the electroencephalographic theta rhythms as well as the amplitude of the intracellular theta oscillations were voltage-dependent. These findings are consistent with the hypothesis that rhythmic GABAA receptor-mediated inhibitory postsynaptic potentials contribute to the genesis of the intracellular theta rhythm. Indeed, mossy cells displayed an early, fast inhibitory postsynaptic potential in response to electrical stimulation of the entorhinal cortex, which most likely represents a GABAA receptor-mediated event, indicating that mossy cells possess functional GABAA receptors. At the resting membrane potential, mossy cells did not fire at each cycle of the electroencephalographic theta rhythm but fired only rarely (< 1 Hz). However, when they did fire they did so preferentially in phase with the peak positivity of the electroencephalographic theta rhythm. Reconstruction of two mossy cells with axonal projections to the inner molecular layer showed that the spatial extent of the influence such weakly discharging mossy cells may have on other dentate gyrus neurons during theta oscillations can be several millimeters in the septotemporal direction. In conclusion, these findings show that mossy cells of the rat hilus during ketamine-xylazine anesthesia participate in theta oscillations of the hippocampal formation, during which their low-frequency firing may contribute to the phase-locking of a large number of spatially distributed postsynaptic neurons with postsynaptic sites in the inner molecular layer of the dentate gyrus.