Abstract
The purpose of the present study was to examine whether zinc-positive and zinc-negative hippocampal neurons in rats differed with respect to their projections to the septum. By combining retrograde axonal transport of the fluorescent tracer Fluoro-Gold with histochemical demonstration of zinc selenide complexes in zinc-containing neurons after intraperitoneal injection of sodium selenite, we were able to visualize the distribution of retrogradely Fluoro-Gold labeled neurons and zinc-containing neurons in the same sections. After unilateral injection of Fluoro-Gold into the rat septum a few retrogradely labeled cells were observed in layer IV of the ipsilateral medial entorhinal area, and numerous labeled cells were observed mainly in the superficial layers of the ipsilateral subicular areas and throughout the CA1 and CA3 pyramidal cell layers, as well as in the contralateral CA3 pyramidal cell layer. Zinc-containing neurons were observed in layers IV–VI of the medial entorhinal area, layers II and III of the parasubiculum, layers II, III and V of presubiculum, and in the superficial CA1 and deep CA3 pyramidal cell layers. Cells double-labeled with Fluoro-Gold and zinc selenide complexes were primarily located in distal (relative to the area dentata) parts of the superficial CA1 pyramidal cell layer and distal parts of the deep CA3 pyramidal cell layer and in layers II and III of presubiculum. Only a very few double-labeled cells were seen in the contralateral CA3. The result demonstrates that the hippocampo-septal projection of rats is a mixture of zinc-positive and zinc-negative fibers. Where-as zinc-negative fibers originate from neurons throughout the hippocampal and retrohippocampal areas, zinc-positive fibers originate from distinct subgroups of zinc-containing cells in different areas and layers.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Amaral DG, Dolorfo C, Alvarez-Royo (1991) Organization of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1:415–435
Beaulieu C, Dyck R, Cynader M (1992) Enrichment of glutamate in zinc-containing terminals of the cat visual cortex. Neuroreport 3:861–864
Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417–537
Caballero-Bleda M, Witter MP (1993) Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: an anterograde tracing study in the rat. J Comp Neurol 328:115–129
Chadwick CW, Choi DW (1990) Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons. J Neurosci 1:108–116
Christensen MK, Frederickson CJ, Danscher G (1992) Retrograde tracing of zinc-containing neurons by selenide ions: a survey of seven selenium compounds. J Histochem Cytochem 40:575–579
Chronister RB, DeFrance JF (1979) Organization of projection neurons of the hippocampus. Exp Neurol 66:509–523
Danscher G (1982) Exogeneous selenium in the brain. Histochemistry 76:281–2932
Frederickson CJ, Hernandez MD, Goik MD, Morton JD, McGinty JF (1988) Loss of zinc staining from hippocampal mossy fibers during kainic acid-induced seizures: a histofluorescence study. Brain Res 480:317–321
Garrett B, Sørensen JC, Slomianka L (1992) Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices. Anat Embryol 185:451–459
Gaykema RPA, van der Kuil J, Hersh LB, Luiten PGM (1991) Patterns of direct projections from the hippocampus to the medial septum-diagonal band complex: anterograde tracing with Phaseolus vulgaris leucoagglutinin combined with immunocytochemistry of choline acetyltransferase. Neuroscience 43:349–360
Haug FMS, Blackstad TW, Simonsen AH, Zimmer J (1971) Timm's sulfide silver reaction for zinc during experimental anterograde degeneration of hippocampal mossy fibers. J Comp Neurol 143:23–32
Hjorth-Simonsen A (1973) Some intrinsic connections of the hippocampus in the rat: an experimental analysis. J Comp Neurol 147:145–162
Hori N, Galeno T, Carpenter DO (1987) Responses of pyriform cortex neurons to excitatory amino acids: voltage dependence, conductance changes, and effects of divalent cations. Cell Mol Neurobiol 7:73–90
Howell GA, Frederickson CJ (1990) A retrograde transport method for mapping zinc-containing fiber systems in the brain. Brain Res 515:277–286
Ishizuka NJ, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295:580–623
Koh JY, Choi DW (1988) Zinc alters excitatory amino acid neurotoxicity on cortical neurons. J Neurosci 8:2164–2171
Köhler C (1985) Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504–522
Mayer ML, Vyklicky L (1989) The action of zinc on synaptic transmission and neuronal excitability in cultures of mouse hippocampus. J Physiol 415:351–365
Nakanishi S (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258:597–603
Peters S, Koh J, Choi DW (1987) Zinc selectively blocks the action of N-Methyl-d-Aspartate on cortical neurons. Science 236:589–592
Rassendren FA, Lory P, Pin JP, Nargeot J (1990) Zinc has opposite effects of NMDA and non-NMDA receptors expressed in Xenopus oocytes. Neuron 4:733–749
Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154
Schwerdtfeger WK, Buhl E (1986) Various types of non-pyramidal hippocampal neurons project to the septum and contralateral hippocampus. Brain Res 386:146–154
Siegel A, Edinger H, Ohgami S (1974) The topographical organization of the hippocampal projection to the septal area: a comparative neuroanatomical analysis in the gerbil, rat, rabbit, and cat. J Comp Neurol 157:359–378
Slomianka L, Danscher G, Frederickson CJ (1990) Labeling of the neurons of origin of zinc-containing pathways by intraperitoneal injections of sodium selenite. Neuroscience 38:843–854
Slomianka L (1992) Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience 48:325–352
Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49–84
Swanson LW, Cowan WM (1979) The connections of the septal region in the rat. J Comp Neurol 186:621–656
Swanson LW, Sawchenko PE, Cowan WM (1980) Evidence that the commissural, associational and septal projections from the hippocampus arise from the same neurons. Brain Res 197:207–212
Tamamaki N, Nojyo Y (1991) Disposition of slab-like modules formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus. J Comp Neurol 291:509–519
Tønder N, Johansen FF, Frederickson CJ, Zimmer J, Diemer NH (1990) Possible role of zinc in the selective degeneration of dentate hilar neurons after cerebral ischemia in the adult rat. Neurosci Lett 109:247–252
Westbrook GL, Mayer ML (1987) Micromolar concentrations of Zn2+ antgonize NMDA and GABA responses of hippocampal neurons. Nature 328:640–643
Witter MP, Ostendorf RH, Groenewegen HJ (1990) Heterogenity in the dorsal subiculum of the rat. Distinct neuronal zones project to different cortical and subcortical targets. Eur J Neurosci 2:718–725
Wong EHF, Kemp JA (1991) Sites for antagonism on the N-methyl-d-aspartate receptor channel complex. Annu Rev Pharmacol Toxicol 31:401–425
Zimmer J (1973) Changes in the Timm sulphide silver staining pattern of the rat hippocampus and fascia dentata following early postnatal deafferentation. Brain Res 64:313–326
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sørensen, J.C., Tønder, N. & Slomianka, L. Zinc-positive afferents to the rat septum originate from distinct subpopulations of zinc-containing neurons in the hippocampal areas and layers. Anat Embryol 188, 107–115 (1993). https://doi.org/10.1007/BF00186245
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00186245