Summary
The time of origin of the neurons in the hilus of the dentate gyrus, in the regio superior and regio inferior of Ammon's horn, and in the following retrohippocampal fields — the subiculum, presubiculum, parasubiculum, medial and lateral entorhinal areas and the perirhinal cortex, has been determined in the rat, by the technique of 3H-thymidine autoradiography. In each field the cells are generated over a limited period of about five days, with the majority being formed in a 24–48 h period. As in the neocortex, the cells in the various hippocampal fields are generated in a distinct “inside-out” sequence with respect to the ependymal zone in which they arise. In addition there are two distinct gradients along the transverse, or dentato-rhinal axis, of the formation. Thus the neurons in the hilar region of the dentate gyrus (including field CA4) tend to arise earlier than the pyramidal cells in the regio inferior, and these in turn, are on average, generated earlier than those in the regio superior or in the subiculum. In the retrohippocampal region there is a comparable gradient extending medially from the perirhinal cortex to the presubiculum, the cells in the lateral entorhinal area being formed, on average, earlier than those in the medial entorhinal cortex, and these, in turn, are generated earlier than those in the para- or presubiculum. There is no evidence for a dorso-ventral (or septotemporal gradient) in any part of the hippocampal formation like that found in the dentate gyrus. Cell counts indicate that there are over 320,000 pyramidal cells in the regio superior (field CA1) and about 150,000 in the regio inferior (fields CA2 and CA3).
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References
Abercrombie, M.: Estimation of nuclear population from sections. Anat. Rec. 94, 239–247 (1946)
Angevine, J.B.: Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. 13, Suppl. 2, 1–70 (1965)
Blackstad, T.W.: Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J. comp. Neurol. 105, 417–538 (1956)
Cowan, W.M., Gottlieb, D.I., Hendrickson, A.E., Price, J.L., Woolsey, T.A.: The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res. 37, 21–51 (1972)
Cowan, W.M., Wann, D.F.: A computer system for the measurement of cell and nuclear sizes. J. Micros. 99, 331–348 (1973)
Fricke, R., Cowan, W.M.: An autoradiographic study of the commissural and ipsilateral hippocampodentate projection in the adult rat. J. comp. Neurol. (1978) (in press)
Gaarskjaer, F.B.: Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells. J. comp. Neurol. 178, 49–72 (1978)
Geneser-Jensen, F.A., Blackstad, T.W.: Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Z. Zellforsch. 114, 460–481 (1971)
Gottlieb, D.I., Cowan, W.M.: Evidence for a temporal factor in the occupation of available synaptic sites during the development of the dentate gyrus. Brain Res. 41, 452–456 (1972)
Gottlieb, D.I., Cowan, W.M.: 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 (1973)
Haberly, L.B., Price, J.L.: Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent area. J. comp. Neurol. 178, 711–740 (1978)
Haug, F.-M.S.: Light microscopical mapping of the hippocampal region, the pyriform cortex and the corticomedial amygdaloid nuclei of the rat with Timm's sulfide silver method. I. Area dentata, hippocampus and subiculum. Z. Anat. Entwickl.-Gesch. 145, 1–27 (1974)
Haug, F.-M.S.: Sulfide silver pattern and cytoarchitectonics of parahippocampal areas in the rat. Special reference to the division of area entorhinalis (area 28) and its demarcation from the pyriform cortex. Adv. Embryol. Cell Biol. 552, 1–73 (1976)
Hendry, I.A.: A method to correct adequately for the change in neuronal size when estimating neuronal numbers after nerve growth factor treatment. J. Neurocytol. 5, 337–349 (1976)
Hjorth-Simonsen, A.: Some intrinsic connections of the hippocampus in the rat: an experimental analysis. J. comp. Neurol. 147, 145–162 (1973)
Kaplan, M.S., Hinds, J.W.: Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197, 1092–1094 (1977)
Konigsmark, B.W.: Methods for the counting of neurons. In: Contemporary research methods in neuroanatomy (W.J.H. Nauta and S.O.E. Ebbesson, eds.). New York: Springer-Verlag 1970
Lorente de Nó, R.: Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46, 113–177 (1934)
Meibach, R.C., Siegel, A.: The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study. Brain Res. 88, 508–512 (1975)
Mellgren, S.I., Geneser-Jensen, F.A.: Distribution of monoamine oxidase in the hippocampal region of the rat. Z. Zellforsch. 124, 354–366 (1972)
Raisman, G., Cowan, W.M., Powell, T.P.S.: The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88, 963–996 (1965)
Schlessinger, A.R., Cowan, W.M., Gottlieb, D.I.: An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. comp. Neurol. 159, 149–175 (1975)
Sikes, R.W., Chronister, R.B., White, L.E., Jr.: Origin of the direct hippocampus-anterior thalamic bundle in the rat: a combined horseradish peroxidase-Golgi analysis. Exp. Neurol. 57, 379–395 (1977)
Steward, O., Scoville, S.H.: Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. comp. Neurol. 169, 347–370 (1976)
Swanson, L.W., Cowan, W.M.: Autoradiographic studies of the development and connections of the septal area in the rat. In: The septal nuclei (J. de France, ed.). New York: Plenum 1976
Swanson, L.W., Cowan, W.M.: An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. comp. Neurol. 172, 49–84 (1977)
Swanson, L.W., Wyss, J.M., Cowan, W.M.: An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J. comp. Neurol. (1978) (in press)
Vaughn, J.E., Matthews, D.A., Barber, R.P., Wimer, C., Wimer, R.E.: Genetically-associated variations in the development of hippocampal pyramidal neurons and mossy fiber connectivity. J. comp. Neurol. 173, 41–52 (1977)
Wimer, C.: A method for estimating nuclear diameters to correct for split nuclei in neuronal counts. Brain Res. 133, 376–381 (1977)
Wyss, J.M., Swanson, L.W., Cowan, W.M.: The organization of the fimbria, dorsal fornix and ventral hippocampal commissure in the rat (in preparation)
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This work was supported in part by research grant NS 10943 from the National Institute of Neurological and Communicative Disorders and Stroke
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Schlessinger, A.R., Cowan, W.M. & Swanson, L.W. The time of origin of neurons in Ammon's horn and the associated retrohippocampal fields. Anat Embryol 154, 153–173 (1978). https://doi.org/10.1007/BF00304660
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DOI: https://doi.org/10.1007/BF00304660