The Entorhinal Cortex Entrains Fast CA1 Hippocampal Oscillations in the Anaesthetized Guinea‐pig: Role of the Monosynaptic Component of the Perforant Path

Entorhinal inputs reach the hippocampal CA1 field through a trisynaptic circuit involving dentate granule cells and CA3 pyramidal neurons, as well as through a monosynaptic path ending on the distal apical dendrites of CA1 pyramidal cells. The influence of monosynaptic entorhinal inputs onto CA1 operations is poorly understood. In this study, we characterized the involvement of the monosynaptic pathway in the generation of the fast CA1 oscillation bursts (30–60 Hz) that occur in the dorsal hippocampus of anaesthetized guinea‐pigs after partial cortex removal. Using multiple‐site extracellular and intracellular recording, we found that in this particular preparation, devoid of theta rhythm, fast oscillations are temporally coherent over a large portion of the CA1 region along the hippocampal septotemporal axis. Current source density analysis revealed that fast CA1 oscillations involve two dipoles reflecting synchronous synaptic activities in the stratum lacunosum‐moleculare of the hippocampus proper and in the stratum moleculare of the dentate gyrus. These layers constitute the two major termination zones of entorhinal afferents, suggesting that the entorhinal cortex entrains fast CA1 oscillations. This hypothesis was corroborated by the concomitant occurrence of fast oscillation bursts in the entorhinal cortex and CA1 region. Furthermore, fast CA1 oscillations were abolished by lidocaine or tetrodotoxin injections in the entorhinal cortex. Finally, acute interruption of the hippocampal trisynaptic loop did not affect the stratum lacunosum‐moleculare dipole recorded extracellularly, but also intracellularly, as high‐frequency postsynaptic potentials in CA1 pyramidal cells. These results indicate that the monosynaptic pathway is involved in the genesis of fast CA1 oscillations.