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Volume 16, Number 12, Issue of June 15, 1996 pp. 3991-4004
Copyright ©1996 Society for Neuroscience

Expression of NGF and NT3 mRNAs in Hippocampal Interneurons Innervated by the GABAergic Septohippocampal Pathway

Received Dec. 19, 1995; revised March 18, 1996; accepted March 21, 1996.

Nativitat Rocamora¹, Marta Pascual¹, Laszlo Acsàdy², Luís de Lecea³, Tamàs F. Freund², and Eduardo Soriano¹

¹ Department of Animal and Plant Cell Biology, Faculty of Biology, University of Barcelona, Barcelona 08028, Spain, ² Institute of Experimental Medicine, Hungarian Academy of Sciences, H-1450 Budapest, Hungary, and ³ Department of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037

We used in situ hybridization for the detection of nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), and neurotrophin 3 (NT3) mRNAs combined with immunocytochemistry against the calcium-binding proteins parvalbumin (PARV), calbindin 28k (CALB), and calretinin (CALR) to determine the expression of neurotrophins in functionally distinct subsets of hippocampal interneurons. Most PARV-immunoreactive neurons in the hippocampus were NGF mRNA-positive (82%), which corresponds to 71% of NGF-positive neurons in the hippocampus proper and in the dentate gyrus (excluding granule cells). In contrast, only a subset of CALB- and CALR-immunoreactive interneurons (24% and 23%, respectively) displayed hybridization signals for NGF. Small subsets of PARV- and CALR-positive cells expressed NT3 mRNA, but we did not find hippocampal interneurons expressing BDNF mRNA. These results show that NGF and NT3 genes are differentially regulated in distinct subsets of GABAergic cells, and these interneurons are a major source of NGF production in the hippocampus.

We also addressed whether hippocampal interneurons expressing neurotrophins were targets of the GABAergic septohippocampal pathway. We developed a triple-labeling method that combines anterograde tracing of this pathway by means of Phaseolus vulgaris leucoagglutinin injections, with in situ hybridization for the detection of neurotrophins, and immunocytochemistry for calcium-binding proteins. Virtually every PARV-positive neuron innervated by GABAergic septohippocampal baskets expressed NGF mRNA (86%), whereas 39-59% of CALR- and CALB-positive interneurons that were contacted by GABAergic septohippocampal axons showed NGF gene expression. A small subset of NT3 mRNA-expressing interneurons was also innervated by septohippocampal baskets. These findings show that the GABAergic septohippocampal pathway preferentially terminates on interneurons expressing NGF mRNA, suggesting that this neurotrophic factor might be involved in the specification of this connection and in its maintenance and normal function in the adult brain.

Key words: rat hippocampus; GABAergic interneurons; neurotrophic factor expression; nerve growth factor; neurotrophin 3; calcium binding proteins; septohippocampal connections; cholinergic afferents

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