Cerebral Cortex pp 167-213 | Cite as
Comparative Anatomy of the Hippocampus
Abstract
Experimental work beginning in the last century and carried on with increasing intensity in recent times has provided ever more precise accounts of the anatomical, physiological, and biochemical properties of the various subfields and interconnections of the hippocampal formation. Indeed, hippocampus is now one of the most thoroughly described regions in mammalian brain. Despite this, it has not been possible to link the specific neurobiological features of the structure to its contributions to behavior; this is quite possibly one of the reasons that the role of hippocampus in processes such as learning and memory remains a subject of continuing controversy.
Keywords
Dentate Gyrus Entorhinal Cortex Molecular Layer Mossy Fiber Perforant PathPreview
Unable to display preview. Download preview PDF.
References
- Altschuler, R. A., Monaghan, D. T., Hasser, W. G., Wenthold, R. J., Curthoys, N. P., and Cotman, C. W., 1985, Immunocytochemical localization of glutaminase-like and aspartate aminotransferase-like immunoreactivities in the rat and guinea pig hippocampus, Brain Res. 330: 225–233.PubMedCrossRefGoogle Scholar
- Amarai, D. G., 1978, A Golgi study of cell types in the hilar region of the hippocampus in the rat, J. Comp. Neurol. 182: 851–914.CrossRefGoogle Scholar
- Amarai, D. G., and Campbell, M. J., 1986, Transmitter systems in the primate dentate gyrus, Hum. Neurobiol. 5: 169–180.Google Scholar
- Amarai, D. G., Insausti, R., and Cowan, W. M., 1984, The commissural connections of the monkey hippocampal formation, J. Comp. Neurol. 224: 307–336.CrossRefGoogle Scholar
- Andersen, P., Bliss, T. V. P., and Skrede, K. K., 1971, Lamellar organization of hippocampal excitatory pathways, Exp. Brain Res. 13: 222–238.Google Scholar
- Andersen, P., Silfvenius, H., Sundberg, S. H., and Sveen, O., 1980, A comparison of distal and proximal dendritic synapses on CAI pyramids in hippocampal slices in vitro, J. Physiol. (London) 307: 273–299.Google Scholar
- Armstrong, E., 1982, A look at relative brain size in mammals, Neurosci. Lett. 34: 101–104.PubMedCrossRefGoogle Scholar
- Bakst, I., and Amarai, D. G., 1984, The distribution of acetylcholinesterase in the hippocampal formation of the monkey, J. Comp. Neurol. 225: 344–371.PubMedCrossRefGoogle Scholar
- Bakst, I., Morrison, J. H., and Amarai, D. G., 1985, The distribution of somatostatin-like immunoreactivity in the monkey hippocampal formation, J. Comp. Neurol. 236: 423–442.PubMedCrossRefGoogle Scholar
- Bakst, I., Avendano, C., Morrison, J. H., and Amarai, D. G., 1986, An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat, J. Neurosci. 6: 1452–1463.PubMedGoogle Scholar
- Barber, R. P., Vaughn, J. E., Wimer, R. E., and Wimer, C. C., 1974, Genetically-associated variations in the distribution of dentate granule cell synapses upon the pyramidal dendrites in mouse hippocampus, J. Comp. Neurol. 156: 417–434.PubMedCrossRefGoogle Scholar
- Bayer, S., 1980, Development of the hippocampal region in the rat: I. Neurogenesis examined with 3H-thymidine autoradiography, J. Comp. Neurol. 190: 87–114.PubMedCrossRefGoogle Scholar
- Blackstad, T. W., 1956, Commissural connections of the hippocampal region of the rat with special reference to their mode of termination, J. Comp. Neurol. 105: 417–538.PubMedCrossRefGoogle Scholar
- Blackstad, T. W, and Kjaerheim, A., 1961, Special axo-dendritic synapses in the hippocampal cortex: Electron and light microscopic studies on the layer of mossy fibers, J. Comp. Neurol. 117: 133–159.PubMedCrossRefGoogle Scholar
- Blackstad, T. W., Brink, K., Hem, J., and Jeune, B., 1970, Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods, J. Comp. Neurol. 138: 443–450.CrossRefGoogle Scholar
- Chan-Palay, V., 1987, Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/silver intensification on vibratome sections: Coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia, J. Comp. Neurol. 260: 201–223.PubMedCrossRefGoogle Scholar
- Chan-Palay, V., Köhler, C., Haesler, U., Lang, W., and Yasargil, G., 1985, Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus, J. Comp. Neurol. 248: 360–375.CrossRefGoogle Scholar
- Chavkin, C., and Bloom, F., 1986, Opiate antagonists do not alter neuronal responses to stimulation of opioid-containing pathways in rat hippocampus, Neuropeptides 7: 19–22.PubMedCrossRefGoogle Scholar
- Chavkin, C., Neumaier, J. F., and Swearengen, E., 1988, Opioid receptor mechanisms in the rat hippocampus, in: Opioids in the Hippocampus, NIDA Research Monograph No. 82 (J. F. McGinty and D. P. Friedman, eds.), pp. 94–117.Google Scholar
- Crain, B. J., Chang, K.-J., and McNamara, J. O., 1986, Quantitative autoradiographic analysis of mu and delta opioid binding sites in the rat hippocampal formation, J. Comp. Neurol. 246: 170–180.PubMedCrossRefGoogle Scholar
- Crawford, I. L., and Connor, J. D., 1973, Localization and release of glutamic acid in relation to the hippocampal mossy fibre pathway, Nature 244: 442–443.PubMedCrossRefGoogle Scholar
- Cuello, A. C., Galfre, G., and Milstein, C., 1979, Detection of substance P in the central nervous system by a monoclonal antibody, Proc. Natl. Acad. Sci. USA 76: 3532–3536.PubMedCrossRefGoogle Scholar
- Davies, S., and Köhler, C., 1985, The substance P innervation of the rat hippocampal region, Anat. Embryol. 173: 45–52.PubMedCrossRefGoogle Scholar
- Del Fiacco, M., Levanti, M. C., Dessi, M. L., and Zucca, G., 1987, The human hippocampal formation and parahippocampal gyrus: Localization of substance P-like immunoreactivity in newborn and adult post-mortem tissue, Neuroscience 21: 141–150.PubMedCrossRefGoogle Scholar
- Demeter, S., Rosene, D. L., and Van Hoesen, G., 1985, Interhemispheric pathways of the hippocampal formation, presubiculum, and entorhinal and posterior parahippocampal cortices in the rhesus monkey: The structure and organization of the hippocampal commissures, J. Comp. Neurol. 233: 30–47.PubMedCrossRefGoogle Scholar
- Dingledine, R., 1981, Possible mechanisms of enkephalin action on hippocampal CAI pyramidal neurons, J. Neurosci. 1: 1022–1035.PubMedGoogle Scholar
- Dodd, J., and Kelly, J. S., 1981, The actions of cholecystokinin and related peptides on pyramidal neurons of the mammalian hippocampus, Brain Res. 205: 337–350.PubMedCrossRefGoogle Scholar
- Dreifuss, J. J., and Raggenbass, M., 1986, Tachykinins and bombesin excite non-pyramidal neurones in rat hippocampus, J. Physiol. (London) 379: 417–428.Google Scholar
- Fitzpatrick, D., and Johnson, R. P., 1981, Enkephalin-like immunoreactivity in the mossy fiber pathway of the hippocampal formation of the tree shrew (Tupaia glis), Neuroscience 6: 2485–2494.PubMedCrossRefGoogle Scholar
- Fredens, K., Stengaard-Pedersen, K., and Larsson, L.-I., 1984, Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields of the rat hippocampal formation, Brain Res. 304: 255–263.PubMedCrossRefGoogle Scholar
- Fredens, K., Stengaard-Pedersen, K., and Wallace, M. N., 1987, Localization of cholecystokinin in the dentate commissural-associational system of the mouse and rat, Brain Res. 401: 68–78.PubMedCrossRefGoogle Scholar
- Fricke, R., and Cowan, W. M., 1978, An autoradiographic study of the commissural and ipsilateral hippocampo-dentate projections in the adult rat, J. Comp. Neurol. 181: 253–270.PubMedCrossRefGoogle Scholar
- Gaarskjaer, F. B., 1978, Organization of the mossy fiber system of the rat studied in extended hippocampi. II. Experimental analysis of fiber distribution with silver impregnation methods, J. Comp. Neurol. 178: 73–88.PubMedCrossRefGoogle Scholar
- Gaarskjaer, F. B., Danscher, G., and West, M. J., 1982, Hippocampal mossy fibers in the regio superior of the European hedgehog, Brain Res. 237: 79–90.PubMedCrossRefGoogle Scholar
- Gall, C., 1984a, The distribution of cholecystokinin-like immunoreactivity in the hippocampal formation of the guinea pig: Localization in the mossy fibers, Brain Res. 306: 73–83.PubMedCrossRefGoogle Scholar
- Gall, C., 1984b, Ontogeny of dynorphin-like immunoreactivity in the hippocampal formation of the rat, Brain Res. 307: 327–331.PubMedCrossRefGoogle Scholar
- Gall, C., 1988a, Localization and seizure-induced alterations of opioid peptides and CCK in the hippocampus, in: Opioids in the Hippocampus, NIDA Research Monograph No. 82 (J. F. McGinty and D. P. Friedman, eds.), pp. 12–32.Google Scholar
- Gall, C., 1988b, Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and cholecystokinin immunoreactivities in mouse hippocampal mossy fibers, J. Neurosci. 8: 1852–1862.PubMedGoogle Scholar
- Gall, C., and Selawski, L., 1984, Supramammillary afferents to guinea pig hippocampus contain substance P-like immunoreactivity, J. Comp. Neurol. 51: 171–176.Google Scholar
- Gall, C., and White, J. D., 1989, Studies on the expression of opioid peptides and their respective mRNAs in hippocampal seizure, in: The Hippocampus: New Vistas ( V. Chan-Palay and C. Kohlër, Alan Liss, New York, pp. 153–170.Google Scholar
- Gall, C., McWilliams, R., and Lynch, G., 1979, The effect of collateral sprouting on the density of innervation of normal target sites: Implications for theories on the regulation of the size of developing synaptic domains, Brain Res. 175: 37–47.PubMedCrossRefGoogle Scholar
- Gall, C., McWilliams, R., and Lynch, G., 1980, Accelerated rates of synaptogenesis by’sprouting’ afferents in the immature hippocampal formation, J. Comp. Neurol. 193: 1047–1063.PubMedCrossRefGoogle Scholar
- Gall, C., Brecha, N., Karten, H. J., and Chang, K.-J., 1981, Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus, J. Comp. Neurol. 198: 335–350.PubMedCrossRefGoogle Scholar
- Gall, C., Berry, L. M., and Hodgson, L. A., 1986a, Cholecystokinin in the mouse hippocampus: Localization in the mossy fiber and dentate commissural systems, Exp. Brain Res. 62: 431–437.PubMedCrossRefGoogle Scholar
- Gall, C., Ivy, G., and Lynch, G., 1986b, Neuroanatomical plasticity: Its role in organizing and reorganizing the central nervous system, in: Human Growth, Volume 2 ( F. Falkner and J. M. Tanner, eds.), Plenum Press, New York, pp. 411–436.Google Scholar
- Gall, C., Lauterborn, J., Burks, D., and Seroogy, K., 1987a, Colocalization of enkephalin and cholecystokinin in discrete areas of rat brain, Brain Res. 403: 403–408.PubMedCrossRefGoogle Scholar
- Gall, C., White, J. D., and Lauterborn, J. C., 1987b, In situ hybridization analyses of increased preproenkephalin mRNA following seizures, Soc. Neurosci. Abstr. 13: 1277.Google Scholar
- Geneser, F. A., 1987, Distribution of acetylcholinesterase in the hippocampal region of the rabbit: III. The dentate area, J. Comp. Neurol. 262: 594–606.PubMedCrossRefGoogle Scholar
- Geneser-Jensen, F. A., Haug, F.-M. S., and Danscher, G., 1974, Distribution of heavy metals in the hippocampal region of the guinea pig. A light microscope study with Timm’s sulfide silver method, Z. Zeilforsch. 147: 441–478.CrossRefGoogle Scholar
- Goldowitz, D., White, W. F., Steward, O., Lynch, G., and Cotman, C., 1975, Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat, Exp. Neurol. 47: 433–441.PubMedCrossRefGoogle Scholar
- Gottlieb, D. I., and Cowan, W M., 1972, Evidence for a temporal factor in the occupation of available synaptic sites during the development of the dentate gyrus, Brain Res. 41: 452–456.PubMedCrossRefGoogle Scholar
- Gottlieb, D. I., and Cowan, W. M., 1973, Autoradiographic studies of the commissural and ipsilateral association connections of the hippocampus and dentate gyrus of the rat. I. The commissural connections, J. Comp. Neurol. 149: 393–422.PubMedCrossRefGoogle Scholar
- Greenwood, R. S., Godar, S., Reaves, T. A., Jr., and Hayward, J., 1981, Cholecystokinin in hippocampal pathways, J. Comp. Neurol. 203: 335–350.PubMedCrossRefGoogle Scholar
- Habets, A. M. M. C., Lopes da Silva, F. H., and de Quartel, F. W, 1980, Autoradiography of an olfactory hippocampal pathway in the cat with special reference to the perforant path, Exp. Brain Res. 38: 257–265.Google Scholar
- Haglund, L., Swanson, L. W, and Köhler, C., 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: 171–185.PubMedCrossRefGoogle Scholar
- Haug, F.-M. S., 1974, Light microscopical mapping of the hippocampal region, the pyriform cortex and the corticomedial amygdaloid nuclei of the rat with Timm’s sulphide silver method. I. Area dentata, hippocampus, and subiculum, Z. Anat. Entwicklungsgesch. 145: 1–27.PubMedCrossRefGoogle Scholar
- Haug. F.-M. S., 1976, Sulphide silver pattern and cytoarchitectonics of parahippocampal areas in the rat, Adv. Anat. Embryol. Cell Bio. 52: 1–73.Google Scholar
- Haug, F. M., Blackstad, T., Hjorth-Simonsen, A., and Zimmer, J., 1971, Timm’s sulfide silver reaction for zinc during experimental anterograde degeneration of hippocampal mossy fibers, J. Comp. Neurol. 142: 23–32.PubMedCrossRefGoogle Scholar
- Hendry, S. H. C., and Jones, E. G., 1985, Morphology of synapses formed by cholecystokinin-immunoreactive axon terminals in regio superior of rat hippocampus, Neuroscience 16: 57–68.PubMedCrossRefGoogle Scholar
- Henriksen, S. J., Wiesner, J. B., and Chouvet, G., 1988, Opioids in the hippocampus: Progress obtained from in vivo electrophysiological analyses, in: Opioids in the Hippocampus, NIDA Research Monograph No. 82 (J. F. McGinty and D. P. Friedman, eds.), pp. 67–93.Google Scholar
- Hjorth-Simonsen, A., 1972a, Some intrinsic connections of the hippocampus in the rat: An experimental analysis, J. Comp. Neurol. 147: 145–161.CrossRefGoogle Scholar
- Hjorth-Simonsen, A., 1972b, Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata, J. Comp. Neurol. 146: 219–232.PubMedCrossRefGoogle Scholar
- Hjorth-Simonsen, A., 1977, Distribution of commissural afferents to the hippocampus of the rabbit, J. Comp. Neurol. 176: 495–514.PubMedCrossRefGoogle Scholar
- Hjorth-Simonsen, A., and Jeune, B., 1972, Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation, J. Comp. Neurol. 144: 215–232.PubMedCrossRefGoogle Scholar
- Hjorth-Simonsen, A., and Laurberg, S., 1977, Commissural connections of the dentate area in the rat, J. Comp. Neurol. 174: 591–606.PubMedCrossRefGoogle Scholar
- Hjorth-Simonsen, A., and Zimmer, J., 1975, Crossed pathways from the entorhinal area to the fascia dentata: I. Normal in rabbits, J. Comp. Neurol. 161: 57–70.PubMedCrossRefGoogle Scholar
- Hong, J.-S., McGinty, J. F., Grimes, L., Kanamatsu, T., Obie, J., and Mitchell, C. L., 1988, Seizure-induced alterations in the metabolism of hippocampal opioid peptides suggest opioid modulation of seizure-related behaviors, in: Opioids in the Hippocampus, NIDA Research Monograph No. 82 (J. F. McGinty and D. P. Friedman, eds.), pp. 48–66.Google Scholar
- Ino, T., Itoh, K., Sugimoto, T., Kaneko, T., Kamiya, H., and Mizuno, N., 1988, The supramammillary region of the cat sends substance P-like immunoreactive axons to the hippocampal formation and the entorhinal cortex, Neurosci. Lett. 90: 259–264.PubMedCrossRefGoogle Scholar
- Jaffe, D. B., Aitken, P. G., and Nadler, J. V., 1987, The effects of cholecystokinin and cholecystokinin antagonists on synaptic function in the CAI region of the rat hippocampal slice, Brain Res. 415: 197–203.PubMedCrossRefGoogle Scholar
- Jan, Y. N., and Jan, L. Y., 1983, Co-existence and co-release of cholinergic and peptidergic transmitters in frog sympathetic ganglia, Fed. Proc. 42: 2929–2933.PubMedGoogle Scholar
- Jerison, H. J., 1973, Evolution of the Brain and Intelligence, Academic Press, New York.Google Scholar
- Jones, E. G., DeFelipe, J., Hendry, S. H. C., and Maggio, J. E., 1988, A study of tachykinin immunoreactive neurons in monkey cerebral cortex, J. Neurosci. 8: 1206–1224.PubMedGoogle Scholar
- Kalivas, P. W., Deutch, A. Y, Maggio, J. E., Mantyh, P. W., and Roth, R. H., 1985, Substance K and substance P in the ventral tegmental area, Neurosci. Lett. 57: 241–246.PubMedCrossRefGoogle Scholar
- Köhler, C., and Chan-Palay, V., 1982, Somatostatin-like immunoreactive neurons in the hippocampus: An immunocytochemical study in the rat, Neurosci. Lett. 34: 259–264.PubMedCrossRefGoogle Scholar
- Köhler, C., Eriksson, L., Davies, S., and Chan-Palay, V., 1986, Neuropeptide Y innervation of the hippocampal region in the rat and monkey brain, J. Comp. Neurol. 244: 384–444.PubMedCrossRefGoogle Scholar
- Kosaka, T., Kosaka, K., Tateishi, K., Hamaoka, Y, Yanaihara, N., Wu, J.-Y, and Hama, K., 1985, Gabaergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus, J. Comp. Neurol. 239: 420–430.PubMedCrossRefGoogle Scholar
- Krettek, J. E., and Price, J. L., 1977, Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat, J. Comp. Neurol. 172: 723–752.PubMedCrossRefGoogle Scholar
- Laatsch, R. H., and Cowan, W. M., 1965, Electron microscopic studies of the dentate gyrus of the rat. I. Normal structure with special reference to synaptic organization, J. Comp. Neurol. 128: 359–396.CrossRefGoogle Scholar
- Laurberg, S., and S0rensen, K. E., 1981, Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3), Brain Res. 212: 287–300.PubMedCrossRefGoogle Scholar
- Laurberg, S., and Zimmer, J., 1980, Aberrant hippocampal mossy fibers in cats, Brain Res. 188: 555–559.PubMedCrossRefGoogle Scholar
- Lorente de Nó, R., 1934, Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system, J. Psychol. Neurol. 46: 113–177.Google Scholar
- Lotstra, F., and Vanderhaeghen, J.-J., 1987, Distribution of immunoreactive cholecystokinin in the human hippocampus, Peptides 8: 911–920.PubMedCrossRefGoogle Scholar
- Lundberg, J. M., and Hökfelt, T., 1986, Multiple co-existence of peptides and classical transmitters in peripheral autonomic and sensory neurons—Functional and pharmacological implications, Prog. Brain Res. 68: 241–262.PubMedCrossRefGoogle Scholar
- Lynch, G., Mosko, S., Parks, T., and Cotman, C., 1973, Relocation and hyperdevelopment of the dentate gyrus commissural system after entorhinal lesions in immature rats, Brain Res. 50: 174–178.PubMedCrossRefGoogle Scholar
- Lynch, G. S., Jensen, R. A., McGaugh, J., Davila, K., and Oliver, M. W., 1981, Effects of enkephalin, morphine and naloxone on the electrical activity of the in vitro hippocampal slice preparation, Exp. Neurol. 71: 527–540.PubMedCrossRefGoogle Scholar
- McGinty, J. F., Henriksen, S., Goldstein, A., Terenius, L., and Bloom, F. E., 1983, Dynorphin is contained within hippocampal mossy fibers: Immunochemical alterations after kainic acid administration and colchicine induced neurotoxicity, Proc. Natl. Acad. Sci. USA 80: 589–593.PubMedCrossRefGoogle Scholar
- McGinty, J. F., Van Der Kooy, D., and Bloom, F. E., 1984, The distribution and morphology of opioid peptide immunoreactive neurons in the cerebral cortex of rats, J. Neurosci. 4: 1104–1117.PubMedGoogle Scholar
- McLean, S., Rothman, R. B., Jacobson, A. E., Rice, K. C., and Herkenham, M., 1987, Distribution of opiate receptor subtypes and enkephalin and dynorphin immunoreactivity in the hippocampus of squirrel, guinea pig, rat, and hamster, J. Comp. Neurol. 255: 497–510.PubMedCrossRefGoogle Scholar
- MacVicar, B. A., Kerrin, J. P., and Davison, J. S., 1987, Inhibition of synaptic transmission in the hippocampus by cholecystokinin (CCK) and its antagonism by a CCK analog (CCK 27–33), Brain Res. 406: 130–135.PubMedCrossRefGoogle Scholar
- Maggio, J. E., and Hunter, J. C., 1985, “Kassinin” in mammals: The newest tachykinin, Peptides 6:(Suppl. 3):237–243.Google Scholar
- Nawa, H., Hirose, T., Takashima, H., Inayaka, S., and Nakanishi, S., 1983, Nucleotide sequences of cloned cDNAs for two types of bovine brain substance P precursor, Nature 306: 32–36.PubMedCrossRefGoogle Scholar
- Nicoli, R. A., 1982, Neurotransmitters can say more than just “yes” and “no,” Trends Neurosci. 5: 369–374.CrossRefGoogle Scholar
- Nicoli, R. A., Siggins, G. R., Ling, N., Bloom, F. E., and Guillemin, R., 1977, Neuronal actions of endorphins and enkephalins among brain regions: A comparative microiontophoretic study, Proc. Natl. Acad. Sci. USA 74: 2584–2588.CrossRefGoogle Scholar
- Nicoli, R., Alger, B., and Jahr, C., 1980, Enkephalin blocks inhibitory pathways in the vertebrate CNS, Nature 287: 22–25.CrossRefGoogle Scholar
- Pohle, W., and Ott, T., 1984, Localization of entorhinal cortex neurons projecting to the dorsal hippocampal formation. A stereotaxic tool in three dimensions, J. Hirnforsch. 25: 661–669.PubMedGoogle Scholar
- Ramón y Cajal, S., 1911, Histologie due Système Nerveux de l’Homme et des Vertébrés, Volume II, Maloine, Paris.Google Scholar
- Ramón y Cajal, S., 1968, The Structure of Ammoris Horn, Thomas, Springfield, 111.Google Scholar
- Rawlins, J. N. P., and Green, K. F., 1977, Lamellar organisation in the rat hippocampus, Exp. Brain Res. 28: 335–344.PubMedCrossRefGoogle Scholar
- Ribak, C. E., and Seress, L., 1983, Five types of basket cell in the hippocampal dentate gyrus. A combined Golgi and electron microscopic study, J. Neurocytol. 12: 577–597.PubMedCrossRefGoogle Scholar
- Rosene, D. L., and Van Hoesen, G. W., 1987, The hippocampal formation of the primate brain: A review of some comparative aspects of cytoarchitecture and connections, in: Cerebral Cortex, Volume 6 ( E. G. Jones and A. Peters, eds.), Plenum Press, New York, pp. 345–356.CrossRefGoogle Scholar
- Ruth, R. E., Collier, T J., and Routtenberg, A., 1982, Topography between the entorhinal cortex and the dentate septotemporal axis in rats: I. Medial and intermediate entorhinal projecting cells, J. Comp. Neurol. 209: 69–78.PubMedCrossRefGoogle Scholar
- Ruth, R. E., Collier, T. J., and Routtenberg, A., 1988, Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats: II. Cells projecting from lateral entorhinal subdivisions, J. Comp. Neurol. 270: 506–516.PubMedCrossRefGoogle Scholar
- Sakamoto, N., Michel, J.-P., Kopp, N., Tohyama, M., and Pearson, J., 1987, Substance P and enkephalin-immunoreactive neurons in the hippocampus and related areas of the human infant brain, Neuroscience 22: 801–811.PubMedCrossRefGoogle Scholar
- Schwerdtfeger, W. K., and Buhl, E., 1986, Various types of non-pyramidal hippocampal neurons project to the septum and contralateral hippocampus, Brain Res. 386: 146–154.PubMedCrossRefGoogle Scholar
- Seress, L., and Mrzljak, L., 1987, Basal dendrites of granule cells are normal features of the fetal and adult dentate gyrus of both monkey and human hippocampal formations, Brain Res. 405: 169–174.PubMedCrossRefGoogle Scholar
- Sloviter, R. S., and Nilaver, G., 1987, Immunocytochemical localization of GABA-, cholecystokinin, vasoactive intestinal polypeptide- and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat, J. Comp. Neurol. 256: 42–60.PubMedCrossRefGoogle Scholar
- Smith, Y., Parent, A., Kerkerian, L., and Pelletire, G., 1985, Distribution of neuropeptide Y immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimirí sciureus), J. Comp. Neurol. 236: 71–89.PubMedCrossRefGoogle Scholar
- Stanfield, B. B., and Cowan, W. M., 1979, The morphology of the hippocampus and dentate gyrus in normal and reeler mice, J. Comp. Neurol. 185: 393–422.PubMedCrossRefGoogle Scholar
- Stanfield, B. B., Caviness, V. S., Jr., and Cowan, W. M., 1979, The organization of certain afferents to the hippocampus and dentate gyrus in normal and reeler mice, J. Comp. Neurol. 185: 461–484.PubMedCrossRefGoogle Scholar
- Stengaard-Pedersen, K., Fredens, K., and Larsson, L. I., 1983, Comparative localization of enkephalin, cholecystokinin and heavy metals in the hippocampus, Brain Res. 273: 81–96.PubMedCrossRefGoogle Scholar
- Stephan, H., and Manolescu, J., 1980, Comparative investigations on hippocampus in insectivores and primates, Z. Mikrosk. Anat. Forsch. 94: 1025–1050.PubMedGoogle Scholar
- Stephan, H., Frahm, H., and Baron, G., 1981, New and revised data on volumes of brain structures in insectivores and primates, Folia Primatol. 35: 1–29.PubMedCrossRefGoogle Scholar
- Steward, O., 1976, Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat, J. Comp. Neurol. 167: 285–314.PubMedCrossRefGoogle Scholar
- Swanson, L. W., Wyss, J. M., and Cowan, W. M., 1978, An autoradiographic study of the organization of the intrahippocampal association pathways in the rat, J. Comp. Neurol. 181: 681–716.PubMedCrossRefGoogle Scholar
- Swanson, L. W., Sawchenko, P. E., and Cowan, W. M., 1981, Evidence for collateral projections by neurons in Ammon’s horn, the dentate gyrus and the subiculum: A multiple retrograde labeling study in the rat, J. Neurosci. 1: 548–559.PubMedGoogle Scholar
- Tielen, A. M., van Leeuwen, F. W., and Lopes da Silva, F. H., 1982, The localization of leucineenkephalin immunoreactivity within guinea pig hippocampus, Exp. Brain Res. 48: 288–295.PubMedCrossRefGoogle Scholar
- Tokimasa, T, Morita, K., and North, A., 1981, Opiates and Clonidine prolong calcium-dependent after-hyperpolarizations, Nature 294: 162–163.PubMedCrossRefGoogle Scholar
- Van Groen, T., and Wyss, J. M., 1988, Species differences in hippocampal commissural connections: Studies in rat, guinea pig, rabbit, and cat, J. Comp. Neurol. 267: 322–334.PubMedCrossRefGoogle Scholar
- Van Hoesen, G. W., and Pandya, D. N., 1975, Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections, Brain Res. 95: 39–59.PubMedCrossRefGoogle Scholar
- Vincent, S. R., Kimura, H., and McGeer, E., 1981, Organization of substance P fibers within the hippocampal formation demonstrated with a biotin-avidin immunoperoxidase technique, J. Comp. Neurol. 199: 113–123.PubMedCrossRefGoogle Scholar
- Walaas, I., 1983, The hippocampus, in: Chemical Neuroanatomy ( P. C. Emson, ed.), Raven Press, New York, pp. 337–358.Google Scholar
- Warden, M. K., and Young, W. S., III, 1988, Distribution of cells containing mRNAs encoding substance P and neurokinin B in the rat central nervous system, J. Comp. Neurol. 272: 90–113.PubMedCrossRefGoogle Scholar
- Watkins, J. C., and Evans, R. H., 1981, Excitatory amino acid transmitters, Annu. Rev. Pharmacol. Toxicol. 21: 165–204.PubMedCrossRefGoogle Scholar
- West, J. R., 1983, Distal infrapyramidal and longitudinal mossy fibers at a midtemporal hippocampal level, Brain Res. Bull. 10: 137–146.PubMedCrossRefGoogle Scholar
- West, J. R., Nornes, H. O., Barnes, C. L., and Bronfenbrenner, M., 1979, The cells of origin of the commissural afferents to the area dentata in the mouse, Brain Res. 160: 203–215.PubMedCrossRefGoogle Scholar
- West, J. R., Van Hoesen, G. W., and Kosel, K. C., 1982, A demonstration of hippocampal mossy fiber axon morphology using anterograde transport of horseradish peroxidase, Exp. Brain Res. 48: 209–216.PubMedCrossRefGoogle Scholar
- West, M. J., and Andersen, A. H., 1980, An allometric study of the area dentata in the rat and mouse, Brain Res. Rev. 2: 317–348.CrossRefGoogle Scholar
- West, M. J., and Schwerdtfeger, W. K., 1985, An allometric study of hippocampal components: A comparative study of the brains of the European hedgehog (Erinaceus europaeus), the tree shrew (Tupaia glis), and the marmoset monkey (Callithrix jacchus), Brain Behau Evol. 27: 93–105.CrossRefGoogle Scholar
- White, J. D., Gall, C. M., and McKelvy, J. F., 1986, Evidence for projection-specific processing of proenkephalin in the rat central nervous system, Proc. Natl. Acad. Sci. USA 83: 7099–7103.PubMedCrossRefGoogle Scholar
- White, J. D., Gall, C. M., and McKelvy, J. F., 1987, Enkephalin biosynthesis and enkephalin gene expression are increased in hippocampal mossy fibers following a unilateral lesion of the hilus, J. Neurosci. 7: 753–759.PubMedGoogle Scholar
- Wiesner, J. B., and Henriksen, S. J., 1987, Enkephalin enhances responsiveness to perforant path input while decreasing spontaneous activity in the dentate gyrus, Neurosci. Lett. 74: 95–101.PubMedCrossRefGoogle Scholar
- Witter, M. P., 1986, A survey of the anatomy of the hippocampal formation, with emphasis on the septotemporal organization of its intrinsic and extrinsic connections, in: Excitatory Amino Acids and Epilepsy ( R. Schwarcz and Y. Ben-Ari, eds.), Plenum Press, New York, pp. 67–82.CrossRefGoogle Scholar
- Witter, M. P., and Groenewegen, H. J., 1984, Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat, J. Comp. Neurol. 224: 371–385.PubMedCrossRefGoogle Scholar
- Witter, M. P., Griffioen, A. W, Jorritsma-Byham, B., and Krijnen, J. L. M., 1988, Entorhinal projections to the hippocampal CAI region in the rat: An underestimated pathway, Neurosci. Lett. 85: 193–198.PubMedCrossRefGoogle Scholar
- Womack, M. D., MacDermott, A. B., and Jessel, T. M., 1988, Sensory transmitters regulate intracellular calcium in dorsal horn neurons, Nature 334: 351–353.PubMedCrossRefGoogle Scholar
- Wyss, J. M., 1981, An autoradiographic study of the efferent connections of the entorhinal cortex in the rat, J. Comp. Neurol. 199: 495–512.PubMedCrossRefGoogle Scholar
- Wyss, J. M., Swanson, L. W, and Cowan, W. M., 1979, Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus, Anat. Embryol. 156: 165–176.PubMedCrossRefGoogle Scholar
- Zieglgansberger, W, French, E. D., Siggins, G. R., and Bloom, F. E., 1979, Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons, Science 205: 415–417.PubMedCrossRefGoogle Scholar
- Zimmer, J., 1971, Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in de-commissurated rats by silver impregnation, J. Comp. Neurol. 142: 393–409.PubMedCrossRefGoogle Scholar
- Zimmer, J., 1973, Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation, Brain Res. 64: 293–311.PubMedCrossRefGoogle Scholar
- Zimmer, J., and Sunde, N., 1984, Neuropeptides and astroglia in intracerebral hippocampal transplants: An immunohistochemical study in the rat, J. Comp. Neurol. 227: 331–347.PubMedCrossRefGoogle Scholar