Summary
Following the injection of a small amount of a labeled amino acid into the hilar region of the dentate gyrus in normal rats, the numbers of silver grains over the supra- and infrapyramidal blades of the dentate gyrus seen in autoradiograms taken at more rostral levels (due to axonal transport in the ipsilateral hippocampo-dentate associational fibers to the inner part of the molecular layer) show a fairly consistent ratio of about 2:1. If the commissural fibers to the same zone (from the hilar region of the contralateral side) are prevented from reaching the dentate gyrus by ablating the contralateral hippocampus and fimbria on the day after birth the corresponding ratio of silver grains is close to 1:1. On the reasonable assumption that the relative numbers of silver grains observed in this type of experiment bear some constant relationship to the relative numbers of labeled axon terminals, these findings suggest that in the absence of commissural afferents, the associational fibers are distributed more-or-less uniformly throughout the “hippocampal zone” of the molecular layer. The simplest interpretation of this is that the associational and commissural afferents normally compete with each other for the available synaptic sites in the hippocampal zone (and especially in the infrapyramidal blade of the dentate gyrus) as postulated by Gottlieb and Cowan (1972), and that when the associational afferents do not have to compete with the commissural fibers, they occupy all the available synaptic sites.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angevine, J.B., Jr.: Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. 13, Suppl. 2, 1–70 (1965)
Coggeshall, R.E., McLean, P.D.: Hippocampal lesions following administration of 3-acetylpyridine. Proc. Soc. Exp. Biol. Med. 98, 687–688 (1958)
Cotman, C.W., Nadler, J.V.: Reactive synaptogenesis in the hippocampus. In: Neuronal plasticity (C.W. Cotman, ed.). New York: Raven Press 1978
Cotman, C., Gentry, C., Steward, O.: Synaptic replacement in the dentate gyrus after unilateral entorhinal lesion: electron microscopic analysis of the extent of replacement of synapses by the remaining entorhinal cortex. J. Neurocytol. 6, 455–464 (1977)
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)
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)
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)
Hendrickson, A.E., Wagoner, N., Cowan, W.M.: An autoradiographic and electron microscopic study of retino-hypothalamic connections. Z. Zellforsch. 135, 1–26 (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)
Hjorth-Simonsen, A., Laurberg, S.: Commissural connections of the dentate area in the rat. J. Comp. Neurol. 174, 591–606 (1977)
Jones, E.G., Hartmann, B.K.: Recent advances in neuroanatomical methodology. Ann. Rev. Neurosci. 1, 215–296 (1978)
Lynch. G., Gall, C., Rose, G., Cotman, C.W.: Changes in the distribution of the dentate gyrus associational system following unilateral or bilateral entorhinal lesions in the adult rat. Brain Res. 110, 57–71 (1976)
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)
Nadler, J.V., Perry, B.W., Cotman, C.W.: Preferential vllnerability of hippocampus to intraventricular kainic acid. In: Kainic acid as a tool in neurobiology (E.G. McGeer, J.W. Olney and P.O. McGeer, eds.). New York: Raven Press 1978
Nafstad, P.H.J.: An electron microscope study on the termination of the perforant path fibres in the hippocampus and the fascia dentata. Z. Zellforsch. 76, 532–542 (1967)
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, 149–176 (1975)
Segal, M.: A potent inhibitory monosynaptic hypothalamo-hippocampal connection. Brain Res. 162, 137–141 (1979)
Sperry, R.W.: Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci USA 50, 703–710 (1963)
Stanfield, B., Cowan, W.M.: Evidence for a change in the retino-hypothalamic projection in the rat following early removal of one eye. Brain Res. 104, 129–136 (1976)
Stanfield, B.B., Cowan, W.M.: The development of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 423–460 (1979a)
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. (Berl.) 156, 37–52 (1979b)
Steward, O., Cotman, C.W., Lynch, G.S.: Growth of a new fiber projection in the brain of adult rats: re-innervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Exp. Brain Res. 20, 45–66 (1974)
Steward, O., Cotman, C.W., Lynch, G.S.: Growth of a new fiber projection in the brain of adult rats: re-innervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions. Exp. Brain Res. 20, 45–66 (1974)
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., Jones, E.G.: An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and cat. J. Comp. Neurol. 156, 143–164 (1974)
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 dentate in the mouse. Brain Res. 160, 203–216 (1979)
Wyss, J.M., Swanson, L.W., Cowan, W.M.: 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 (Berl.) 156, 165–176 (1979)
Zimmer, J.: Ipsilateral afferents to the commissural zone of the fascia dentata, domonstrated in decommissurated rats by silver impregnantion. J. Comp. Neurol. 142, 393–416 (1971)
Zimmer, J.: Proximity as a factor in the regulation of aberrant axonal growth in postnatally deafferented fascia dentata. Brain Res. 72, 137–142 (1974)
Zimmer, J., Haug, F.-M.Š.: Laminar differentiation of the hippocampus, fascia dentata and subculum 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 from the National Institutes of Health and DA-00259 from ADAMAH
Supported by Training Grant EY-00092
Rights and permissions
About this article
Cite this article
O'Leary, D.D.M., Fricke, R.A., Stanfield, B.B. et al. Changes in the associational afferents to the dentate gyrus in the absence of its commissural input. Anat Embryol 156, 283–299 (1979). https://doi.org/10.1007/BF00299628
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00299628