Summary
Fragments of the dentate gyrus containing portions of the stratum granulosum and the overlying stratum moleculare were isolated from their commissural, associational and hypothalamic inputs in 11 and 28-day-old rats. Six weeks later the distribution of the entorhinal afferents to the isolated portion of the stratum moleculare was determined autoradiographically by the injection of 3H-proline into the medial entorhinal area, and the appearance of the molecular layer was examined in Timm's sulfide silver preparations. It is evident from our material that under these circumstances the entorhinal afferents to the dentate gyrus can extend right up to the stratum granulosum and that the normal staining pattern that characterizes the “hippocampal zone” of the molecular layer in Timm's preparations may disappear and be replaced, in part, by a narrow zone of dense, mossy fiber-like staining.
The simplest interpretation of these findings is that fibers from the medial entorhinal area are capable of sprouting into the deafferented “hippocampal zone” of the dentate gyrus. However, the observation that entorhinal afferents may occupy the entire thickness of the molecular layer does not, by itself, establish this point because in every case examined the whole molecular layer was shrunken. While this calls for some caution in the interpretation of the findings, our results suggest that there is no special barrier to the growth of entorhinal fibers and that the inner part of molecular layer of the dentate gyrus is capable of receiving afferents other than those normally present.
Similar content being viewed by others
References
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)
Cajal, S., Ramón y: The structure of Ammon's horn. (English translation of Cajal, 1893) Springfield, Illinois: Charles C Thomas, 1968
Cotman, C.W., Nadler, J.V.: Reactive synaptogenesis in the hippocampus. In: Neuronal plasticity, (C.W.Cotman, ed.), pp. 227–271. New York: Raven Press 1978
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)
Devor, M.: Neuroplasticity in the rearrangement of olfactory tract fibers after neonatal transection in hamsters. J. Comp. Neurol. 166, 49–72 (1976)
Fricke, R.A.: Studies of the morphology and development of the dentate gyrus. Doctoral dissertation, Washington University, St. Louis, Missouri 1975
Fricke, R., Cowan, W.M.: An autoradiographic study of the development of the entorhinal and commissural afferents to the dentate gyrus of the rat. J. Comp. Neurol. 173, 231–250 (1977)
Fricke, R., Cowan, W.M.: An autoradiographic study of the commissural and ipsilateral hippocampo-dentate projections in the adult rat. J. comp. Neurol. 181, 253–270 (1978)
Goldowitz, D., White, W.I., Steward, O., Lynch, G., Cotman, C.: Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Exp. Neurol. 47, 433–441 (1975)
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)
Haug, F.-M.Š.: Electron microscopical localization of the zinc in hippocampal mossy fibre synapses by a modified sulfide silver procedure. Histochemie 8, 355–368 (1967)
Haug, F.-M.Š.: Heaby metals in the brain. A light microscopy study of the rat with Timm's sulphide silver method. Methodological considerations and cytological and regional staining patterns. Advances in Anatomy, Embryology and Cell Biology 47, 1–71 (1973)
Haug, F.-M.Š.: 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. Entwickl.-Gesch. 145, 1–27 (1974)
Haug, F.-M.Š., Blackstad, T.W., Simonsen, A.H., Zimmer, J.: Timm's sulfide silver reaction for zinc during experimental anterograde degeneration of hippocampal mossy fibers. J. Comp. Neurol. 142, 23–32 (1971)
Hjorth-Simonsen, A.: Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neurol. 146, 219–232 (1972)
Hjorth-Simonsen, A., Jeune, B.: Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144, 215–232 (1972)
Ibata, Y., Otsuka, N.: Electron microscopic demonstration of zinc in the hippocampal formation using Timm's sulfide-silver technique. J. Histochem. Cytochem. 17, 171–175 (1969)
Jones, B.E., Moore, R.Y.: Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study. Brain Res. 127, 23–53 (1977)
Krieg, W.J.S.: Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas. J. Comp. Neurol. 84, 221–276 (1946a)
Krieg, W.J.S.: Connections of the cerebral cortex. I. The albino rat. B. Structure of the cortical areas. J. Comp. Neurol. 84, 277–323 (1946b)
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)
Loy, R., Lynch, G., Cotman, C.W.: Development of afferent lamination in the fascia dentata of the rat. Brain Res. 121, 229–243 (1977)
Lynch, G., Gall, C., Cotman, C.: Temporal parameters of axon “sprouting” in the brain of the adult rat. Exp. Neurol. 54, 179–183 (1977)
Lynch, G., Gall, C., Rose, G., Cotman, C.W.: Changes in the distribution of the dentate gyrus associational system following unilateral or bilateral entorhinal lesion in the adult rat. Brain Res. 110, 57–71 (1976)
Lynch, G.S., Mosko, S., Parks, T., Cotman, C.W.: Relocation and hyperdevelopment of the dentate gyrus commissural system after entorhinal lesions in immature rats. Brain Res. 50, 174–178 (1973a)
Lynch, G., Stanfield, B., Cotman, C.W.: Developmental differences in post-lesion axonal growth in the hippocampus. Brain Res. 59, 155–168 (1973b)
Lynch, G., Stanfield, B., Parks, T., Cotman, C.W.: Evidence for selective post-lesion axonal growth in the dentate gyrus of the rat. Brain Res. 69, 1–11 (1974)
McWilliams, R., Lynch, G.: Terminal proliferation and synaptogenesis following partial deafferentation: the reinnervation of the inner molecular layer of the dentate gyrus following removal of its commissural afferents. J. Comp. Neurol. 180, 581–616 (1978)
Moore, R.Y.: Monoamine neurons innervating the hippocampal formation and septum. In: The hippocampus (K.H. Pribram and R.L. Isaacson, eds.). New York: Plenum Press 1975
Moore, R.Y., Halaris, A.E.: Hippocampal innervation by serotonin neurons in the midbrain raphe in the rat. J. Comp. Neurol. 164, 171–184 (1975)
Raisman, G., Cowan, W.M., Powell, T.P.S.: The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88, 963–996 (1965)
Steward, O.: Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 167, 285–314 (1976)
Steward, O., Cotman, C., Lynch, G.: A quantitative autoradiographic and electrophysiological study of the reinnervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Brain Res. 114, 181–200 (1976)
Swanson, L.W., Cowan, W.M.: The connections of the septal region in the rat. J. Comp. Neurol. (In press) 1979
Swanson, L.W., Hartman, B.K.: The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-β-hydroxylase as a marker. J. Comp. Neurol. 163, 467–506 (1975)
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. 181, 681–715 (1978)
West, J.R., Nornes, H.O., Barnes, C.L., Bronfenbrenner, M.: The cells of origin of the commissural afferents to the area dentata in the mouse. Brain Res. 160, 203–216 (1979)
Wyss, J.M., Swanson, L.W., Cowan, W.M.: Evidence for an additional input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat. Embryol. (In press) 1979
Zimmer, J.: Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J. Comp. Neurol. 142, 393–416 (1971)
Zimmer, J.: Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64, 293–311 (1973a)
Zimmer, J.: Changes in the Timm-sulfide silver staining pattern of the rat hippocampus and fascia dentata following early postnatal deafferentation. Brain Res. 64, 313–326 (1973b)
Zimmer, J.: Proximity as a factor in the regulation of aberrant axonal growth in postnatally deafferented fascia dentata. Brain Res. 72, 137–142 (1974a)
Zimmer, J.: Long term synaptic reorganization in rat fascia dentata deafferented at adolescent and adult stages: Observations with the Timm method. Brain Res. 76, 137–142 (1974b)
Zimmer, J., Haug, F.-M.Š.: Laminar differentiation of the hippocampus, fascia dentata and subiculum in developing rats, observed with the Timm sulphide silver method. J. Comp. Neurol. 179, 581–618 (1978)
Zimmer, J., Hjorth-Simonsen, A.: Crossed pathways from the entorhinal area to the fascia dentata. II. Provokable in rats. J. Comp. Neurol. 161, 71–102 (1975)
Author information
Authors and Affiliations
Additional information
This work was supported in part by grants NS-10943 and EY-01255 from the National Institutes of Health
Rights and permissions
About this article
Cite this article
Stanfield, B., Cowan, W.M. Evidence for the sprouting of entorhinal afferents into the “hippocampal zone” of the molecular layer of the dentate gyrus. Anat Embryol 156, 37–52 (1979). https://doi.org/10.1007/BF00315714
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00315714