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Volume 16, Number 10, Issue of May 15, 1996 pp. 3322-3333
Copyright ©1996 Society for Neuroscience

A Novel Entorhinal Projection to the Rat Dentate Gyrus: Direct Innervation of Proximal Dendrites and Cell Bodies of Granule Cells and GABAergic Neurons

Received Nov. 2, 1995; revised Feb. 12, 1996; accepted Feb. 19, 1996.

Thomas Deller¹, Albert Martinez², Robert Nitsch³, and Michael Frotscher¹

¹ Institute of Anatomy, University of Freiburg, D-79001 Freiburg, Germany, ² Departamento de Biologia Cellular Animal i Vegetal, Universitat de Barcelona, 08028 Barcelona, Spain, and ³ Institute of Anatomy, Humboldt University Clinic (Charité), 10098 Berlin, Germany

Entorhinal fibers to the fascia dentata originating from layer II stellate neurons are known to terminate exclusively in the outer two thirds of the molecular layer, where they innervate distal dendritic portions of dentate neurons. Using anterograde tracing with Phaseolus vulgaris leucoagglutinin, we unraveled a previously unknown entorhinal projection that directly innervates proximal dendritic portions and somata of granule cells and GABAergic neurons. This projection originates from neurons located in entorhinal layers IV-VI of the medial entorhinal area. These fibers enter the outer two thirds of the molecular layer, traverse the inner molecular layer (IML) and granule cell layer, where they form numerous boutons, and finally arborize subjacent to the granule cells. Correlated light and electron microscopy revealed that the boutons formed by these fibers establish asymmetric synapses on dendrites in the IML, on spines and somata of granule cells, and on spineless dendrites subjacent to the granule cell layer. Postembedding immunogold staining indicates that this entorhino-dentate projection is not GABAergic and that it also terminates on GABAergic inhibitory neurons. These data demonstrate that not all entorhino-dentate fibers display a similar high laminar specificity for the outer molecular layer (OML). Although fibers from the superficial layers of the entorhinal cortex terminate exclusively in the OML, entorhinal fibers arising from deeper layers are not confined to laminar boundaries. Finally, the possibility that these supposedly excitatory entorhinal afferents may monosynaptically activate proximal dendrites and somata of dentate neurons needs to be incorporated into contemporary concepts of the hippocampal network.

Key words: entorhino-hippocampal interaction; perforant pathway; feedforward inhibition; GABA-postembedding; laminar specificity; Phaseolus vulgaris leucoagglutinin

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