A Survey of the Anatomy of the Hippocampal Formation, with Emphasis on the Septotemporal Organization of Its Intrinsic and Extrinsic Connections

  • M. P. Witter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 203)


The hippocampal formation (HF) is composed of the hippocampus proper, i.e., the cornu Ammonis (CA) and the fascia dentata (FD), and the subiculum (Sub). Despite a rather extensive knowledge of its extrinsic and intrinsic connections, the functions of the HF are still an enigma. The suggestion has been made that the hippocampus contains a map of the external spatial environment, but also that it plays a more general role in memory and learning processes (O’Keefe and Nadel, 1978; Olton et al., 1982; Olton, 1983; Squire, 1983). A most relevant notion as regards the subject of this symposium is that the HF has long been implicated in temporal lobe epilepsy. Already in 1880, Sommer reported that many epileptic patients showed extensive loss of neurons, in particular in field CA1 of the CA. Recently, the anatomy of the hippocampal circuitry in relation to the occurrence of seizures has attracted special attention (Somogyi et al., 1983a, b). Although it appears that the basic circuitry is similar in all parts of the hippocampus, the present analysis of the topographical organization of the major intrinsic and extrinsic connections suggests that different parts along the septotemporal axis of the HF are connected with a different set of extra-hippocampal structures (Ruth et al., 1982; Roberts et al., 1984;. Witter and Groenewegen, 1984; Van Groen and Lopes da Silva, 1985).


Entorhinal Cortex Hippocampal Formation Mossy Fiber Perirhinal Cortex Cornu Ammonis 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amaral, D.G., 1978, A Golgi study of cell types in the hilar region of the hippocampus in the rat, J, Comm, Neurol., 182: 851.Google Scholar
  2. Amaral, D.G., and Cowan, W.M., 1980, Subcortical afferents to the hippocampal formation in the monkey, J. Comm. Neurol., 189: 573.Google Scholar
  3. Amaral, D.G., Insausti, R., and Cowan, W.M., 1984, The commissural connec-tions of the monkey hippocampal formation, J. Comm. Neurol., 224:307. Andersen, P., Bliss, T.V.P., and Skrede, K.K., 1971, Lamellar organization of hippocampal excitatory pathways, Exm. Brain Rea., 13: 222.Google Scholar
  4. Ashwood, T.J., Lancaster, B., and Wheal, H.V., 1984, In vivo and in vitro,studies on putative interneurons in the rat hippocampus: possiblemediators of feed-forward inhibition, Brain Res,, 293: 279.PubMedCrossRefGoogle Scholar
  5. Azmitia, E.C., and Segal, M., 1978, An autoradiographic analysis of the differential ascending projections of the dorsal and the median raphenuclei in the rat, J. Comm. Neurol., 179: 641.Google Scholar
  6. Bakst, I., Morrison, J.H., and Amaral, D.G., 1985, The distribution of somatostatin-like immunoreactivity in the monkey hippocampal formation, J. Comm. Neurol., 236: 423.Google Scholar
  7. Berger, T.W., Swanson, G.W., Milner, T.A., Lynch, G.S., and Thompson, R.F., 1980, Reciprocal anatomical connections between hippocampus and subiculum in the rabbit: evidence for subicular innervation of regio superior, Brain Res., 183: 265.PubMedCrossRefGoogle Scholar
  8. Blackstad, T.W., 1956, Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination, J. Comm. Neurol„ 105: 417.Google Scholar
  9. 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. Como. Neurol,, 138: 433.Google Scholar
  10. Buzsaki, G., 1984, Feed-forward inhibition in the hippocampal formation, Progress in Neurobiol., 22: 131.CrossRefGoogle Scholar
  11. Chandler, J.P., and Crutcher, H.A., 1983, The septohippocampal projection in the rat: an electronmicroscopic horseradish peroxidase study, Neuroscience, 10: 685.PubMedCrossRefGoogle Scholar
  12. Crunelli, V., and Segal, M., 1985, An electrophysiological study of neurones in the rat median raphe and their projections to septum and hippocampus, Neuroscience, 15: 47.PubMedCrossRefGoogle Scholar
  13. Crutcher, H.A., Madison, R., and Davis, J.N., 1981, A study of the rat septohippocampal pathway using anterograde transport of horseradish peroxidase, Neuroscience, 6: 1961.PubMedCrossRefGoogle Scholar
  14. Demeter, S., Rosene, D.L., and Van Hoesen, G.W., 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. Çomv. Neurol., 233: 30.Google Scholar
  15. Dent, J.A., Galvin, N.J., Stanfield, B.B., and Cowan, W.M., 1983, The mode of termination of the hypothalamic projection to the dentate gyrus: an EM autoradiographie study, Brain Res., 258: 1.CrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. Fricke, R., and Cowan, W.M., 1978, Autoradiographic study of the commissural and ipsilateral hippocampal-dentate projections in the adult rat, J. Como. Neurol„ 181: 253.Google Scholar
  18. Frotscher, M., and Zimmer, J., 1983, Commissural fibers terminate on non-pyramidal neurons in the guinea pig hippocampus. A combined Golgi/EM degeneration study, Brain Res., 265: 289.Google Scholar
  19. Frotscher, M., Leranth, Cs., Lubbers, K., and Oertel, W.H., 1984, Commissural afferents innervate glutamate decarboxylase immunoreactive non-pyramidal neurons in the guinea pig hippocampus, Neurosci. Lett., 46: 137.Google Scholar
  20. Gage, F.H., and Thompson, R.G., 1980, Differential distribution of norepinephrine and serotonin along the dorso-ventral axis of the hippocampal formation, Brain Res. Bull., 5: 771.Google Scholar
  21. 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. Como. Neurol., 198: 335.Google Scholar
  22. Gall, C., 1984, The distribution of cholecystokinin-like immunoreactivity in the hippocampal formation of the guinea pig: localization in the mossy fibers, Brain Res., 306: 73.PubMedCrossRefGoogle Scholar
  23. 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. Como. Neurol,, 149: 393.Google Scholar
  24. Groenewegen, H.J., Arnolds, D.E.A.T., and Lopes da Silva, F.H., 1981, Afferent connections of the nucleus accumbens in the cat, with special emphasis on the projections from the hippocampal region. An anatomical and electrophysiological study, in: The Neurobiology of the Nucleus Acoumbens, R.B. Chronister, and J.F. De France, eds., Hear Institute for Electrophysiological Res., Brunswick, p. 41.Google Scholar
  25. Groenewegen, H.J., Room, P., Witter, M.P., and Lohman, A.H.M., 1982, Cortical afferents of the nucleus accumbens in the cat, studied with anterograde and retrograde transport techniques, Neuroscience, 7: 977.PubMedCrossRefGoogle Scholar
  26. Groenewegen, H.J., Haber, S.N., and Nauta, W.J.H., 1983, Structure and efferent connections of the interpeduncular nucleus in the rat. An immunohistochemical and neuroanatomical tracer study, Neurosci. Lett. Spool., 14: 145.Google Scholar
  27. 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.Google Scholar
  28. Herkenham, M., 1978, The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat, J. Comp. Neurol,, 177: 589.Google Scholar
  29. 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
  30. 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.Google Scholar
  31. Kelley, A.B., and Domesick, V.B., 1982, The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat:an anterograde- and retrograde-horseradish peroxidase study, Neuroscience, 7: 2321.PubMedCrossRefGoogle Scholar
  32. Knowles, W.D., and Schwartzkroin, P.A., 1981, Local circuit synaptic interactions in hippocampal brain slices, J. Neurosci., 1: 318.PubMedGoogle Scholar
  33. Köhler, C., 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
  34. Köhler, C., 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
  35. Köhler, C., Haglund, L., and Swanson, L.W., 1984, A diffuse a-MSH-immunoreactive projection to the hippocampus and spinal cord from individualneurons in the lateral hypothalamic area and zona incerta, J. Comp. Neurol., 223: 501.Google Scholar
  36. Köhler, C., 1985, Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex, J. Çomp, Neurol., 236: 504.Google Scholar
  37. Kosel, K.C., Van Hoesen, G.W., and Rosene, D.L., 1983, A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat, Brain. Res,, 269: 347.Google Scholar
  38. Krayniak, P.F., Siegel, A., Meibach, R.C., Fruchturan, D., and Scrimenti, M., 1979, Origin of the fornix system in the squirrel monkey, Brain. Res,,, 160: 401.Google Scholar
  39. Krayniak, P.F., Weiner, S., and Siegel, A., 1980, An analysis of the efferent connections of the septal area in the cat, Brain Rea., 189: 15.CrossRefGoogle Scholar
  40. 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.Google Scholar
  41. Laurberg, S., 1979, Commissural and intrinsic connections of the rat hippo-campus, J. Comp. Neurol., 184: 685.Google Scholar
  42. Laurberg, S., and Sirensen, K.E., 1981, Associational and commissural collaterals of neurons in the hippocampal formation (hilus fascia dentatae and subfield CA3), Brain Res., 212: 287.PubMedCrossRefGoogle Scholar
  43. Leichnetz, G.R., and Astruc, J., 1975, Efferent connections of the orbito- frontal cortex in the marmoset ( Saauinus oedipus ), Brain Res., 84: 169.Google Scholar
  44. Leichnetz, G.R., and Astruc, J., 1976, The efferent projections of the medial prefrontal cortex in the squirrel monkey ( Saimiri sciureus ), Brain Res., 109: 455.Google Scholar
  45. Leranth, Cs., and Frotscher. M., 1983, Commissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons. An EM immunocytochemical degeneration study, Brain Res., 276: 357.Google Scholar
  46. Lopes da Silva, F.H., Arnolds, D.E.A.T., and Neijt, H.C., 1984, A functional link between the limbic cortex and ventral striatum: physiology of the subiculum accumbens pathway, Exp. Brain Res., 55: 205.Google Scholar
  47. Lopes da Silva, F.H., Groenewegen, H.J., Hoisheimer, J., Room, P., Witter, M.P., Van Groen, Th., and Wadman, W.J., 1985, The hippocampus as a set of partially overlapping segments with a topographically organized system of inputs and outputs: the entorhinal cortex as a sensory gate, the medial septum as a gain-setting system and the ventral striatum as a motor interface, in: Electrical Activity of the Archicortex,Buzsaki and C.H. VanderWolf, eds., Akademiai Kiado, Budapest, p. 83.Google Scholar
  48. Lorente de Nó, R., 1934, Studies on the structure of the cerebral cortex.Continuation of the study of the ammonic system, Psycho. Neurol., 46: 113.Google Scholar
  49. McNaughton, B.L., 1980, Evidence for two physiologically distinct perforant pathways to the fascia dentata, Brain Res., 199: 1.PubMedCrossRefGoogle Scholar
  50. Meibach, R.C., and Siegel, A., 1977a, Efferent connections of the hippocampal formation in the rat, Brain Res., 124: 197.PubMedCrossRefGoogle Scholar
  51. Meibach, R.C., and Siegel, A., 1977b, Thalamic projections of the hippocampal formation: evidence for an alternate pathway involving the internal capsule, Brain Res., 134: 1.PubMedCrossRefGoogle Scholar
  52. Miles, R., Wong, R.K.S., and Traub, R.D., 1984, Synchronized afterdischarges in the hippocampus: contribution of local synaptic interactions, Neuroscience, 12: 1179.PubMedCrossRefGoogle Scholar
  53. Monmaur, P., and Thomson, M.A., 1983, Topographic organization of septal cells innervating the dorsal hippocampal formation of the rat: special reference to both the CA1 and dentata theta generators, Exp. Neurol., 82: 366.Google Scholar
  54. Newman, R., and Winans, S.S., 1980, An experimental study of the ventral striatum of the golden hamster. I. Neuronal connections of the nucleus accumbens, J. Comp. Neurol., 191: 167.Google Scholar
  55. Nunzi, M.G., Gorio, A., Milan, F., Freund, T.F., Somogyi, P., and Smith, A.D., 1985, Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus,J. Comp. Neurol., 237: 485.Google Scholar
  56. O’Keefe, J., and Nadel, L., 1978, The Hippocampus as a Cognitive Map, Clarendon Press, Oxford.Google Scholar
  57. Olton, D.S., Walker, J.A., and Wolf, W.A., 1982, A disconnection analysis of hippocampal function, Brain Res., 233: 241.PubMedCrossRefGoogle Scholar
  58. Olton, D.S., 1983, Memory functions and the hippocampus, in: Neurobiology of the HipDO0amous, W. Seifert, ed., Academic Press, London, p. 335.Google Scholar
  59. Pasquier, D.A., and Reinoso-Suarez, F., 1976, Direct projections from hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase, Brain Res,., 108: 165.PubMedCrossRefGoogle Scholar
  60. Pasquier, D.A., and Reinoso-Suarez, F., 1977, Differential efferent connections of the brain stem to the hippocampus in the cat, Brain Res., 120: 540.PubMedCrossRefGoogle Scholar
  61. Pasquier, D.A., and Reinoso-Suarez, F., 1978, The topographic organization of hypothalamic and brainstem projections to the hippocampus, Brain Res. Bull., 3: 373.Google Scholar
  62. 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.Google Scholar
  63. 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
  64. 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
  65. Room, P., Russchen, F.T., Groenewegen, H.J., and Lohman, A.H.M., 1985, Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices. An anterograde tracing study in the cat, J, Comp. Neurol., 242: 40.Google Scholar
  66. Room, P., and Groenewegen, H.J., 1986, Connections of the parahippocampal cortex in the cat. I. Cortical afferents, J. Comp. Neurol., in press.Google Scholar
  67. Rosene, D.L., and Van Hoesen, G.W., 1977, Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey, Science, 198: 315.PubMedCrossRefGoogle Scholar
  68. Russchen, F.T., 1982, Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques, J. Comp, Neurol., 206: 159.Google Scholar
  69. 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.Google Scholar
  70. Schwartzkroin, P.A., and Kunkel, D.D., 1985, Morphology of identified interneurons in the CA1 region of guinea pig hippocampus, J. Comp. Neurol., 232: 205.Google Scholar
  71. Schwerdtfeger, W.K., 1984, Structure and fiber connections of the hippocampus. A comparative study, Adv. Anat. Embrvol. Cell. Biol., 83: 1.CrossRefGoogle Scholar
  72. Segal, M., and Landis, S., 1974, Afferents to the hippocampus of the rat studied with the method of retrograde transport of horseradish peroxidase, Brain Res., 78: 1.PubMedCrossRefGoogle Scholar
  73. Segal, M., 1979, A potent inhibitory monosynaptic hypothalamo-hippocampal connection, Brain Res., 162: 137.PubMedCrossRefGoogle Scholar
  74. Siegel, A., and Tassoni, J.P., 1971a, Differential efferent projections from the ventral and dorsal hippocampus of the cat, Brain Behay. Evol., 4: 185.Google Scholar
  75. Siegel, A., and Tassoni, J.P., 1971b, Differential efferent projections of the lateral and medial septal nuclei to the hippocampus in the cat, Brain Behay. Evol., 4: 201.Google Scholar
  76. Siegel, A., Edinger, H., and Ohgami, S., 1974, The topographical organization of the hippocampal projection to the septal area: a comparative neuro-anatomical analysis in the gerbil, rat, rabbit, and cat, J, Comp. Neurol., 157: 359.Google Scholar
  77. Somogyi, P., Nunzi, M.G., Gorio, A., and Smith, A.D., 1983a, A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells, Brain Res., 259: 137.PubMedCrossRefGoogle Scholar
  78. Somogyi, P., Smith, A.D., Nunzi, M.G., Gorio, A., Takagi, H., and Wu, J.Y., 1983b, Glutamate decarboxylase immunoreactivity in the hippocampus of the cat, J. Neurosci., 3: 1450.PubMedGoogle Scholar
  79. Sorensen, K.E., and Shipley, M.T., 1979, Projections from the subiculum to the deep layers of the ipsilateral presubicular and entorhinal cortices in the guinea pig, J. Comp. Neurol., 188: 313.Google Scholar
  80. Squire, L.R., 1983, The hippocampus and the neuropsychology of memory, in: The Neurobiology of the Hippocampus, W. Seifert, ed., Academic Press, London, p. 491.Google Scholar
  81. Stanfield, R.B., Wyss, J.M., and Cowan, W.M., 1980, The projection of the supramammillary region upon the dentate gyrus in normal and reeler mice, Brain Res., 198: 196.PubMedCrossRefGoogle Scholar
  82. Steward, 0., 1976, Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat, J. Comp. Neurol., 167: 285.CrossRefGoogle Scholar
  83. Steward, 0., 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
  84. Struble, R.G., Desmond, N.L., and Levy, W.B., 1978, Anatomical evidence for interlamellar inhibition in the fascia dentata, Brain Res., 152: 580.PubMedCrossRefGoogle Scholar
  85. Swanson, L.W., and Cowan, W.M., 1977, An autoradiographic study of the organzition of the efferent connections of the hippocampal formation in the rat, J. Comp. Neurol., 172: 49.Google Scholar
  86. Swanson, L.W., Wyss, J.M., and Cowan, W.M., 1978, An autoradiographic study of the organization of intrahippocampal association pathways in the rat, J. Comp. Neurol., 181: 681.Google Scholar
  87. Swanson, L.W., and Cowan, W.M., 1979, The connections of the septal region in the rat, J. Comp. Neurol., 186: 621.Google Scholar
  88. Swanson, L.W., Sawchenko, P.E., and Cowan, W.M., 1980, Evidence that the commissural, associational and septal projections of the regio inferior of the hippocampus arise from the same neurons, Brain Res., 197: 207.PubMedCrossRefGoogle Scholar
  89. Swanson, L.W., 1981, A direct projection from Ammon’s horn to prefrontal cortex in the rat, Brain Res., 217: 150.PubMedCrossRefGoogle Scholar
  90. Swanson, L.W., Sawchenko, P.E., and Cowan, W.M., 1981, Evidence for colla- teral projections by neurons in Ammon’s horn, the dentate gyrus and the subiculum. A multiple retrograde labeling study in the rat, J. Neuro-sci., 1: 548.Google Scholar
  91. Taxt, T., and Storm-Mathisen, J., 1984, Uptake of D-aspartate and L-glutamate in excitatory axon terminals in hippocampus: autoradiographic and biochemical comparison with y-aminobutyrate and other amino acids in normal rats and in rats with lesion, Neuroscience, 11: 79.PubMedCrossRefGoogle Scholar
  92. Van Groen, Th., and Lopes da Silva, F.H., 1985, Septotemporal distribution of entorhinal projections to the hippocampus in the cat: electrophysiological evidence, J. Comp. Neurol., 238: 1.Google Scholar
  93. Van Groen, Th., and Witter, M.P., 1985, Electrophysiological and tracing study of the septotemporal distribution of entorhinal projections to the hippocampus in the cat, in: Electrical Activity of Archicortex, G. Buzsaki and C.H. VanderWolf, eds., Academiai Kiado, Budapest, p. 107.Google Scholar
  94. Van Groen, Th., and Lopes da Silva, F.H., 1986, The organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat. II. An electrophysiological study, J. Comp. Neurol., in press.Google Scholar
  95. Van Groen, Th., van Haren, F., Witter, M.P., and Groenewegen, H.J., 1986, The organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat. I. A neuroanatomical tracing study, J. Comp. Neurol., in press.Google Scholar
  96. 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.Google Scholar
  97. Van Hoesen, G.W., Rosene, D.L., and Mesulam, M.-M., 1979, Subicular input from temporal cortex in the rhesus monkey, Science, 205: 608.PubMedCrossRefGoogle Scholar
  98. Van Hoesen, G.W., 1982, The parahippocampal gyrus. New observations regarding its cortical connections in the monkey, TINS, 5: 345.Google Scholar
  99. Veazey, R.B., Amaral, D.G., and Cowan, W.M., 1982, The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). H. Efferent connections, J. Comp. Neurol., 207: 135.Google Scholar
  100. Vincent, S.R., McIntosh, C.H.S., Buchan, A.M.J., and Brown, J.G., 1985, Central somatostatin systems revealed with monoclonal antibodies, J. Comp. Neurol., 238: 169.Google Scholar
  101. Walaas, I., 1983, The hippocampus, in: Chemical Neuroanatomy, P.C. Emson, ed., Raven Press, New York, p. 337.Google Scholar
  102. 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.Google Scholar
  103. Witter, M.P., Room, P., Groenewegen, H.J., and Lohman, A.H.M., 1986, Connections of the parahippocampal cortex in the rat. V. Intrinsic connections; comments on input/output connections with the hippocampus, J. Comp. Neurol., in press.Google Scholar
  104. Wyss, J.M., Swanson, L.W., and Cowan, W.M., 1979a, A study of subcortical afferents to the hippocampal formation in the rat, Neuroscience, 4: 463.PubMedCrossRefGoogle Scholar
  105. Wyss, J.M., Swanson, L.W., and Cowan, W.M., 1979b, Evidence for an input to the molecular layer and the stratum granulosum of the dentata gyrus from the supramammillary region of the hypothalamus, Anat. Embrvol., 156: 165.Google Scholar
  106. Wyss, J.M., 1981, An autoradiographic study of the efferent connections of the entorhinal cortex in the rat, J. Comp. Neurol., 199: 495.Google Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • M. P. Witter
    • 1
  1. 1.Department of AnatomyVrije UniversiteitAmsterdamThe Netherlands

Personalised recommendations