Advertisement

Cytochemical Architecture of the Entorhinal Area

  • Ch. Köhler
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 203)

Abstract

The hippocampal region1) consists of serially arranged cortical fields which become increasingly simplified in their basic laminar structure as one proceeds from the entorhinal area (EA) to the area dentata (Swanson, 1982b; Fig. 1). The EA is the largest retrohippocampal subfield and it gives rise to one of the most prominent association pathways within the entire hippocampal region. This pathway, the perforant path, originates primarily from stellate and pyramidal cells in layers II and III of the medial and the lateral EA, and terminates in the dentate gyrus where it synapses onto the granular cell dendrites in the outer two-thirds of the molecular layer (Blackstad, 1958; Hjorth-Simonsen, 1971; Steward and Scoville, 1976). The medial EA, in turn, receives a topographically organized input from the subfields of the subicular complex: the deep layers of the EA are innervated by the subiculum proper and the outer three layers by the para- and presubiculum, respectively (Shipley, 1975; Köhler, 1985). It is through these latter projections that thalamic as well as some commissural inputs are relayed to the EA, and the association pathways from the subicular complex to the medial EA represent important routes through which afferents of extra-hippocampal origin may affect neurotransmission along the perforant path.

Keywords

Vasoactive Intestinal Peptide Vasoactive Intestinal Polypeptide Glutamic Acid Decarboxylase Hippocampal Region Perforant Path 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen, S., Adrian, T.E., Allen, J.M., Tatemoto, K., Crow, T.J., Bloom, S.R., and Polak, J.M., 1983, Neuropeptide Y distribution in the rat brain, Science, 221: 877.PubMedCrossRefGoogle Scholar
  2. Alonso, A., and 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.Google Scholar
  3. Andersen, P., Holmquist, B., and Voorhoeve, P.E., 1966, Entorhinal activation of dentate granule cells, Acta Physiol. Scand., 66: 448.Google Scholar
  4. Andersen, P., Bliss, T.V.P., and Skrede, K.K., 1971, Lamellar organization of hippocampal excitatory pathways, Exp. Brain Res., 13: 222.Google Scholar
  5. Andersen, P., Bie, B., and Ganes, T., 1982, Distribution of GABA sensitive areas on hippocampal pyramidal cells, Exp. Brain Res., 45: 357.Google Scholar
  6. Blackstad, T.W., 1958, On the termination of some afferents to the hippocampus and fascia dentata. An experimental study in the rat, Acta Anat. 35: 202.Google Scholar
  7. Björklund, A., and Lindvall, 0., 1984, Dopamine-containing systems in the CNS, in: Handbook of Chemical Neuroanatomv, Vol. 2, Part 1, Classi- cal Transmitters in the CNS, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam, p. 55.Google Scholar
  8. Charkin, Ch., Shoemaker, W.J., McGinty, J.F., Bayon, A., and Bloom, F.E., 1985, Characterization of the prodynorphin and proenkephalin neuropeptide systems in rat hippocampus, J. Neurosci., 5: 808.Google Scholar
  9. Chronwell, B.M., Chase, T.N., O’Donohue, T., 1984, Co-existence of neuropeptide Y and somatostatin in human cortical and rat hypothalamic neurons, Neurosci. Lett., 52: 213.Google Scholar
  10. Davies, S., and Köhler, Ch., 1985, The substance P innervation of the hippocampus in the rat, Anat. Embrvol., 173: 45.Google Scholar
  11. Emson, P.C., and Hunt, S.P., 1984, Peptide-containing neurons of the cerebral cortex, in: Cerebral Cortex, Vol. 2, Functional Properties of Cortical Cells, E.G. Jones and A. Peters, eds., Raven Press, New York, p. 145.CrossRefGoogle Scholar
  12. Fredens, K., Stengaard-Pedersen, K., and Larsson, L.-I., 1984, Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields in the rat hippocampal formation, Brain Res., 304: 255.PubMedCrossRefGoogle Scholar
  13. Gall, C., Brecha, N., Karten, H.J., and Chang, K.-I., 1981, Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus, J, Comp, Neurol., 198: 335.Google Scholar
  14. Gall, C., and Selawaski, 1984, Supramammillary efferents to guinea pig hippocampus contain substance P-like immunoreactivity, Neurosci. Lett., 51: 171.Google Scholar
  15. Greenwood, R.S., Godar, S., Reaves, T.A., and Haywood, J.N., 1982, Cholecystokinin in hippocampal pathways, J. Comp. Neurol., 198: 335.Google Scholar
  16. Haglund, L., Swanson, L.W., and Köhler, Ch., 1984, The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat, J. Comp. Neurol., 229: 171.Google Scholar
  17. Handelman, G.E., Meyer, D.U., Beinfeld, M.C., and Oertel, W.H., 1981, CCK-containing terminals in the hippocampus are derived from intrinsic neurons. An immunohistochemical and radioimmunological study, Brain Res., 224: 181.Google Scholar
  18. Hendry, S.H.C., Jones, E.G., DeFelipe, J., Schmechel, D., Brandon,and Emson, P.C., 1984, Neuropeptide containing neurons of the cerebral cortex are also GABAergic, Proc. Natl. Acad. Sci. USA, 81: 6526.Google Scholar
  19. Hjorth-Simonsen, A., 1971, Hippocampal efferents to the ipsilateral entorhi- nal area: an experimental study in the rat, J. Comp. Neurol., 142: 417.Google Scholar
  20. Hökfelt, T., Fahrenkrug, J., Tatemoto, K., and Mutt, V., 1982, PHI, a VIP-like peptide, is present in the rat median eminence, Acta Physiol. Scand., 78: 6603.Google Scholar
  21. Houser, C.R., Vaughn, J.E., Hendry, S.H.C., Jones, E.G., and Peters, A., 1984, GABA neurons in the cerebral cortex, in: Cerebral Cortex, Vol. 2, Functional Properties of Cortical Cells, E.G. Jones and A. Peters,eds., Raven Press, New York, p. 63.CrossRefGoogle Scholar
  22. Itoh, N., Obata, K.-I., Yanaihara, N., and Okamoto, H., 1983, Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27, Nature, 304: 547.PubMedCrossRefGoogle Scholar
  23. Jones, E.G., and Hendry, S.H.C., 1984, Basket cells, in: Cerebral Cortex, Vol, 1, Cellular Components of the Cerebral Cortex, A. Peters and E.G. Jones, eds., Raven Press, New York. p. 309.CrossRefGoogle Scholar
  24. Köhler, Ch., Chan-Palay, V., and Steinbusch, H., 1981, The distribution and orientation of serotonin fibers in the entorhinal and other retrohippocampal areas. An immunohistochemical study with anti-serotonin antibodies in the rat’s brain, Anat. Embrvol., 161: 237.Google Scholar
  25. Köhler, Ch., and Eriksson, L.C., 1981, Efferent projections from the entorhinal area to the basal forebrain and frontal cortex originates in layer IV, Soc. Neurosci, Abstr., 8: 420.Google Scholar
  26. Köhler, Ch., and Chan-Palay, V., 1982, The distribution of cholecystokininlike immunoreactive neurons and nerve terminals in the retrohippocampal region in the rat and guinea pig, J. Comp. Neurol., 210: 136.Google Scholar
  27. Köhler, Ch., and Steinbusch, H., 1982, Identification of serotonin and non-serotonin containing neurons of the mid-brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain, Neuroscience, 7: 951.Google Scholar
  28. Köhler, Ch., 1983, A morphological analysis of vasoactive intestinal polypeptide (VIP)-like immunoreactive neurons in the area dentata of the rat brain, J. Comp. Neurol., 221: 247.Google Scholar
  29. Köhler, Ch., and Chan-Palay, V., 1983a, Distribution of gamma-aminobutyric acid containing neurons and terminals in the septal area. An immunohistochemical study using antibodies to glutamic acid decarboxylase in the rat brain, Anat. Embryol., 167: 53.Google Scholar
  30. Köhler, Ch., and Chan-Palay, V., 1983b, Somatostatin and vasoactive intestinal polypeptide-like immunoreactive cells and terminals in the retrohippocampal region of the rat brain, Anat. Embryol., 167: 151.Google Scholar
  31. Köhler, Ch., Chan-Palay, V., and Wu, J.-Y., 1984a, Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain, Anat. Embryol., 169: 41.Google Scholar
  32. Köhler, Ch., Haglund, L., and Swanson, L.W., 1984b, A diffuse aMSH-immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta, J. Comp. Neurol., 223: 501.Google Scholar
  33. Köhler, Ch., 1985, Intrinsic connections of the retrohippocampal region in the rat’s brain. I. The subicular complex, J. Comp. Neurol., 236: 504.Google Scholar
  34. Köhler, Ch., Chan-Palay, V., and Wu, J.-Y., 1985a, Neurons and terminals in the retrohippocampal region in the rat’s brain identified by anti-y-aminobutyric acid and anti-glutamic acid decarboxylase immunocytochemistry, Anat. Embryol., 173: 35.Google Scholar
  35. Köhler, Ch. Eriksson, L., Davies, S., and Chan-Palay, V., 1985b, Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain, J. Comp. Neurol., in press.Google Scholar
  36. Köhler, Ch., Haglund, L., Swanson, L.W., and Wu, J.-Y., 1985c, The cytoarchitecture, histochemistry and projections of the tubero-manxillary nucleus in the rat brain, Neuroscience, 16: 85.PubMedCrossRefGoogle Scholar
  37. Leranth, C.S., Frotscher, M., Tömbold, T., and Palkovits, M., 1984, Ultra-structure and synaptic connections of vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons and axon terminals in the rat hippocampus, Neuroscience, 12: 531.PubMedCrossRefGoogle Scholar
  38. Loran, I., Emson, P.C., Fahrenkrug, J., Björklund, A., Alumets, J., Hâkansson, R., and Sundler, F., 1976, Distribution of vasoactive intestinal polypeptide in the rat and mouse brain, Neuroscience, 4: 1935.Google Scholar
  39. Lorente de Nó, R., 1934, Studies on the structure of the cerebral cortex, II. Continuation of the study of the Ammonic system, J. Psvchol. Neurol., 46: 113.Google Scholar
  40. McDonald, J.F., Parnavelas, J.G., Karamanlidis, A.N., and Brecha, N., 1982, The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. H. Vasoactive intestinal polypeptide, J. Neurocvtol., 11: 825.Google Scholar
  41. Mesulam, M.M., and Van Hoesen, G.W., 1976, Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to the neocortex, Brain Res., 109: 152.PubMedCrossRefGoogle Scholar
  42. Moore, R.Y., and Card, P.J., 1984, Noradrenaline-containing neuron systems, in: Handbook of Chemical Neuroanatomv, Vol. 2, Part 1, Classical Transmitters in the CNS, A. Björklund and T. Hökfelt, eds., Elsevier, Amsterdam, p. 123.Google Scholar
  43. Peters, A., Miller, M., and Kimmerer, L.M., 1983, Cholecystokinin-like immunoreactive neurons in rat cerebral cortex, Neurosci., 8: 431.CrossRefGoogle Scholar
  44. Peters, A., and Saint Marie, R.L., 1984, Smooth and sparsely spinous non-pyramidal cells forming local axonal plexuses, in: Cerebral Cortex, Vol. 1, Cellular Components of the Cerebral Cortex, A. Peters and E.G. Jones, eds., Raven Press, New York, p. 419.Google Scholar
  45. Ramon y Cajal, S.R., 1911, Histologie du Systeme Nerveux de l’homme et des vertebrates, Vol. II, A. Maloine, Paris.Google Scholar
  46. Ribak, C.E., Vaughn, J.E., and Saito, K., 1978, Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport, Brain Res., 140: 315.PubMedCrossRefGoogle Scholar
  47. Roberts, G.W., Woodhams, P.L., Polak, J.M., and Crow, T.J., 1984, Distribution of neuropeptides in the limbic system of the rat: the hippocampus, Neuroscience, 11: 35.PubMedCrossRefGoogle Scholar
  48. Seress, L., and Ribak, C.E., 1983, GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons, Exp. Brain, Res., 50: 173.Google Scholar
  49. Shipley, M.T., 1975, The topographical and laminar organization of the presubiculum’s projection to the ipsi- and contralateral entorhinal cortex in the guinea pig, J. Comp. Neurol., 160: 127.Google Scholar
  50. Somogyi, P., Cowey, A., Kisvarday, Z.F, Freund, T.F., and Szentagothai, J., 1983a, Retrograde transport of ‘H-GABA reveals specific interlaminar connections in the striate cortex of the monkey, Proc. Natl. Acad. Sci. USA, 80: 2385.Google Scholar
  51. Somogyi, P., Smith, A.D., Nunzi, M.G., Gorio, A., Takagi, H., and WuGoogle Scholar
  52. J.-Y., 1983b, Glutamate decarboxylase immunoreactivity in the hippocampus of the cat. Distribution of immunoreactive terminals with special reference to the axon initial segment of pyramidal neurons, J. Neurosci., 3: 1450.Google Scholar
  53. Somogyi, P., Freund, T.F., Hodgson, A.J., Somogyi, J., Beroukas, D., and Chubb, I.W., 1985, Identified axo-axonic cells are immunoreactive for GAGA in the hippocampus and visual cortex of the cat, Brain Res., 332: 143.PubMedCrossRefGoogle Scholar
  54. Steward, O., and Scoville, S.A., 1976, Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat, J. Comp. Neurol., 169: 347.Google Scholar
  55. Storm-Mathisen, J., 1977, Glutamic acid and excitatory nerve endings: reduction of glutamic acid uptake after axotomy, Brain Res., 120: 379.PubMedCrossRefGoogle Scholar
  56. Streit, P., 1984, Glutamate and aspartate as transmitter candidates for systems of the cerebral cortex, in: Cerebral Cortex, Vol. 2, Functional Properties of Cortical Cells, E.G. Jones and A. Peters, eds., Raven Press, New York, p. 119.CrossRefGoogle Scholar
  57. Swanson, L.W., and Hartman, B., 1975, The central adrenergic system: an immunofluorescent study of the localization of cell bodies and their efferent connections in the rat utilizing dopamine-p-hydroxylase as a marker, J. Comp. Neurol., 163: 467.Google Scholar
  58. Swanson, L.W., 1982a, The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat, Brain Res. Bull., 9: 321.Google Scholar
  59. Swanson, L.W., 1982b, The anatomy of the septo-hippocampal pathway, in: Alzheimers Disease. A Report of Progress. Ageing, Vol. 19, S. Corkin, et al., eds., Raven Press, New York.Google Scholar
  60. Swanson, L.W., Sawchenko, P.E., Rivier, J., and Vale, W.W., 1983, Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study, Neuroendocrinology, 36: 165.PubMedCrossRefGoogle Scholar
  61. Tatemoto, K., and Mutt, V., 1981, Isolation and characterization of the intestinal peptide porcine PHI (PHI-27), a new member of the glucagon secretion family, Proc. Natl. Acad. Sci. USA, 78: 6603.Google Scholar
  62. Tatemoto, K., 1982, Neuropeptide Y: complete amino acid sequence of the brain peptide, Proc. Natl. Acad. Sci. USA, 79: 5485.Google Scholar
  63. Wyss, J.M., Swanson, L.W., and Cowan, W.M., 1979, A study of subcortical afferents to the hippocampal formation in the rat, Neuroscience, 4: 463.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • Ch. Köhler
    • 1
  1. 1.Department of NeuropharmacologyAstra Läkemedel ABSödertäljeSweden

Personalised recommendations