Summary
The distribution of substance P (SP) immunoreactive nerve cell bodies and preterminal processes was studied in the rat brain by using several anti-SP-antibodies in combination with immunohistochemical techniques. In normal rats and in rats pretreated with colchicine, SP immunoreactive preterminal processes were found in the hippocampal region, but SP positive cellbodies could be detected only after colchicine pretreatment. Medium-sized to large, multipolar cells immunoreactive for SP were found in stratum oriens of the hippocampal subfield CA3 and in the hilus of the area dentata. Medium-sized to small, round or fusiform cells were detected in the pyramidal layer of the ventral subiculum and in layers III–VI of the ventral entorhinal area. The SP stained preterminal processes were of two types. Numerous fine, varicose axons were stained in different parts of Ammon's horn, while in the retrohippocampal structures, the SP immunoreactivity was present in small distinctly stained puncta. These frequently formed pericellular arrangements around unstained cells, indicative of axosomatic contacts between SP terminals and cells in the hipocampus. In Ammon's horn, the densest SP innervation was found in strata oriens, radiatum and moleculare of subfields CA3a and CA2. Scattered fibers were also present in the stratum oriens of CA3a-c and in the hilus, in particular at ventral levels. In retrohippocampal structures, the SP innervation predominated in the deep pyramidal layer of the subiculum, the second layer of the presubiculum and in layers VI and IV of the medial and lateral entorhinal area. Many of these terminals may arise from local interneurons as well as from sources outside the hippocampal region.
Taken together, these studies demonstrate a far more extensive innervation by SP, or a closely related peptide, of the rat hippocampal region than was previously recognized. This suggests that SP may play an important role in neurotransmission within the hippocampal region.
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References
Alonso A, Köhler Ch (1984) A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J Comp Neurol 225:327–344
Armstrong DM, Saper CB, Levey AI, Wainer BM, Terry RD (1983) Distribution of cholinergic neurons in the rat brain demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 216:53–68
Coons AH (1954) Fluorescence antibody methods. In J.F. Danielli (ed): General cytochemical methods, New York: Academic Press, pp 399–442
Gall G, Brecha N (1984) Ontogeny of enkephalin-like immunoreactivity in the rat hippocampus. Neuroscience 11:359–380
Gall C, Selawski L (1984) Supramammillary efferents to guinea pig hippocampus contain substance P-like immunoreactivity. Neurosci Lett 51:171–1076
Gall C, Brecha N, Karten HJ, Chang KJ (1981) Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J Comp Neurol 198:335–350
Greenwood RS, Godar S, Reaves TA, Haywar JN (1982) Cholecystokinin in hippocampal pathways. Comp Neurol 203:335–351
Haglund L, Swanson LW, Köhler Ch (1984) The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and antergrade transport study with the lectin PHA-L in the rat. J Comp Neurol 229:171–186
Handelman GE, Meyer DU, Beinfeld MC, Oertel WH (1981) CCK-containing terminals in the hippocampus are derived from intrinsic neurons. An immunohistochemical and radioimmunological study. Brain Res 224:181–185
Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-perioxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabelled antibody (PAP) procedures. J Histochem Cytochem 29:577–580
Johansson O, Backman J (1983) Enhancement of immunoperoxidase staining using osmium tetroxide. J Neurosci Meth 7:185–193
Kanazawa I, Jessel T (1976) Postmortem changes and regional distribution of substance P in the rat and mouse nervous system. Brain Res 117:326–367
Köhler Ch, Chan-Palay V (1983) Somatostain and vasoactive intestinal polypeptide-like immunoreactive cells and terminals in the retrohippocampal region of the rat brain. Anat Embryol 167:151–172
Köhler Ch (1982) Distribution and morphology of vasoactive intestinal polypeptide-like immunoreactive neurons in regio superior of the rat hippocampal formation. Neurosci Lett 33:265–270
Köhler Ch (1983) A morphological analysis of vasoactive intestinal polypeptide (VIP)-like neurons in the area dentata of the rat brain. J Comp Neurol 221:247–262
Köhler Ch, Chan-Palay V (1982a) The distribution of cholecystokinin-like immunoreactive neurons and nerve-terminals in the retrohippocampal region in the rat and guinea pig. J Comp Neurol 210:136–146
Köhler Ch, Chan-Palay V (1982b) Somatostatin-like immunoreactive neurons in the hippocampus: an immunocytochemical study in the rat. Neurosci Lett 34:259–264
Köhler Ch, Haglund L, Swanson LW (1984) A diffuse α-MSH immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta. J Comp Neurol 223:501–514
Köhler Ch, Swanson LW, Wu J-Y (1985) The cytoarchitecture, histochemistry and projections of the tuberomammillary nucleus in the rat. Neuroscience (in press)
Ljungdahl A, Hökfelt T, Nilsson G (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve-terminals. Neuroscience 3:861–943
Mantyh PW, Hunt SP, Maggio JE (1984) Substance P receptors: localization by light microscopic autoradiography in rat brain using [3H] SP as the radioligand. Brain Res 307:147–165
McGinty JF, Hendriksen SJ, Goldstein A, Terenius L, Bloom FE (1983) Dynorphin is contained within hippocampal mossyfibers: immunochemical alterations after kainic acid administration and colchicine induced neurotoxicity. Proc Natl Acad Sci (USA) 80:589–593
McLean I, Nakane P (1974) Periodate-lysine paraformaldehyde fixative: a new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083
Morrison JH, Benoit R, Magistretti PJ, Ling N, Bloom FE (1982) Immunohistochemical distribution of pro-somatostatin-related peptides in hippocampus. Neurosci Lett 34:137–142
Nawa H, Hirose T, Takashima H, Inayama S, Nakamishi S (1983) Nucleotide sequences for cloned cDNAs for two types of bovine substance P precursor. Nature 306:32–36
Nicoll RA, Schenker C, Leeman SE (1980) Substance P as a transmitter candidate. Ann Rev Neurosci 3:227–268
Pepeu G, Mulas A, Ruffi A, Satqui P (1971) Brain acetylocholine levels in rats with septal lesions. Brain Res 10:181–184
Roberts GW, Woodhams PL, Polak JM, Crow TJ (1984) Distribution of neuropeptides in the limbic system of the rat: the hippocampus. Neuroscience 11:35–77
Stengaard-Pedersen K, Fredens K and Karsson L-I (1983) Comparative localization of enkephalin and cholecystokinin immunoreactivities and heavy metals in the hippocampus. Brain Res 273:81–96
Vincent SR, McGeer EG (1981) A substance P projection to the hippocampus. Brain Res 215:349–351
Vincent SR, Kimura H, McGeer EG (1981) Organization of substance P fibers within the hippocampal formation demonstrated with a biotin-avidin immunoperoxidase technique. J Comp Neurol 199:113–123
Von Euler US, Gaddum JH (1931) An unidentified depressor substance in certain tissue extracts. J. Physiol (Lond.) 72:74–87
Von Euler US (1977) Substance P In: Nobel: Symposium 37: Pernow B (Ed.) Raven Press, New York
Wyss JM, Swanson LW, Cowan MW (1979) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463–476
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Stephen Davies was supported by Travel grants from the Wellcome Trust and the Gurantors of Brain.
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Davies, S., Köhler, C. The substance P innervation of the rat hippocampal region. Anat Embryol 173, 45–52 (1985). https://doi.org/10.1007/BF00707303
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DOI: https://doi.org/10.1007/BF00707303