Activation of perforant path neurons to field CA1 by hippocampal projections

AbstractPrevious evidence showed that single‐shock stimulation of dorsal hippocampal commissure (PSD) fibers to the entorhinal cortex led to sequential activation of perforant path neurons to the dentate gyrus, dentate granule cells, pyramidal neurons of hippocampal fields CA3 and CA1, and, through reentrant hippocampal impulses, neurons of deep and superficial layers of the entorhinal cortex. The aim of the present study was to ascertain whether perforant path neurons to CA1 are activated by the PSD input and/or by the reentrant hippocampal impulses in this model. Field potentials evoked by single‐shock (0.1‐Hz) or repetitive (1–4 Hz) PSD stimulation were recorded in anesthetized guinea pigs from the entorhinal cortex, dentate gyrus, fields CA1 and CA3, and subiculum. A current source‐density analysis of the evoked potentials was used to localize the input to field CA1 and dentate gyrus. After either single‐shock or repetitive PSD stimulation, an early current sink was found in the molecular layer of the dentate gyrus, but no sink was present in CA1. With low‐frequency PSD stimulation, a late (∼40‐ms) surface positive wave occurred in field CA1 alone. During this wave, a current sink was found in the stratum lacunosum‐moleculare of CA1, but no sink was present in the dentate gyrus. The late wave had threshold and magnitude related to the building up of the response evoked by reentrant hippocampal impulses in layer III of the entorhinal cortex and was abolished by selective interruption of the perforant path to CA1. The results show that the commissural input to the entorhinal cortex activates perforant path neurons to the dentate gyrus, but not those to field CA1 which are recruited by repetitive hippocampal impulses. These findings show different frequency‐dependent patterns of loop operation that might be related to different behaviors. Hippocampus 2003;13:235–249. © 2003 Wiley‐Liss, Inc.