Summary
Following destruction of the ipsilateral temporo-ammonic tract, which originates in the entorhinal cortex, and terminates on the granule cells of the dentate gyrus, fibers from the surviving contralateral entorhinal area proliferate forming extensive new connections with the denervated dentate granule cells. Utilizing extracellular recording techniques, we have compared the characteristics of synaptic transmission in the lesion induced afferents with the characteristics of the normal ipsilateral afferents by analyzing the responses of dentate granule cells to paired pulse activation of temporo-dentate circuitry.
In the dentate gyrus of the normal rat, an extracellularly recorded EPSP evoked by stimulation of the ipsilateral entorhinal cortex is enhanced by as much as 100% by a “conditioning” pulse to the same afferent system. This is called paired pulse potentiation. In the reinnervated dentate gyrus, the extracellular EPSP evoked by a test stimulus delivered to the contralateral entorhinal cortex is also potentiated by a conditioning pulse. The paired pulse potentiation in the reinnervated dentate gyrus has a time course which is comparable to that of the normal ipsilateral afferent system, but the magnitude of the potentiation is somewhat less, averaging approximately 140% of control.
A second manifestation of paired pulse potentiation in the normal ipsilateral temporo-dentate circuit is that more granule cells discharge in response to the second of a pair of stimuli. Potentiation of granule cell discharge, as measured by the increase in the size of the population spike in the test response, may be as much as 500% of control at the optimal interstimulus interval. In the operated animals, however, paired pulse stimulation of the lesion induced crossed temporo-dentate circuit results in little, if any, enhancement of granule cell discharge in response to the second stimulus, despite the fact that theextracellulrly recorded EPSP is potentiated.
These results are discussed in relation to the similarity between the normal and the lesion induced afferents to the dentate cells, with consideration for the normal functioning of the circuit from the entorhinal cortex to the dentate gyrus.
Similar content being viewed by others
References
Andersen, P., Bliss, T.V.P., Skriede, D.D.: Unit analysis of hippocampal population spikes. Exp. Brain Res. 13, 208–221 (1971)
Andersen, P., Lømo, T.: Mode of control of hippocampal pyramidal cell discharges. In: The Neural Control of Behavior. (eds. R.E. Whalen, R.F. Thompson, M. Verzeano, N.M. Weinberger). pp. 3–26. New York: Academic Press 1970
Bliss, T.V.P., Gardner-Medwin, A.R.: Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 357–374 (1973)
Bliss, T.V.P., Lømo, T.: Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 331–356 (1973)
Cotman, C.W., Matthews, D.A., Taylor, D., Lynch, G.: Synaptic rearrangement in the dentate gyrus: Histochemical evidence of adjustments after lesions in immature and adult rats. Proc. nat. Acad. Sci. (Wash.) 70, 3473–3477 (1973)
Goldowitz, D., White, W.F., Steward, O., Cotman, C., Lynch, G.: Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Exp. Neurol. 47, 433–441 (1975)
Lømo, T.: Patterns of activation in a monosynaptic cortical pathway: The perforant path input to the dentate area of the hippocampal formation. Exp. Brain Res. 12, 18–45 (1971a)
Lømo, T.: Potentiation of monosynaptic EPSP's in the perforant path dentate granule cell synapse. Exp. Brain Res. 12, 46–63 (1971b)
Lynch, G., Deadwyler, S.A., Cotman, C.W.: Post-lesion axonal growth produces permanent functional connections. Science 180, 1364–1366 (1973)
Lynch, G., Matthew, D.A., Mosko, S., Parks, T., Cotman, C.W.: Induced acetylcholinesterase-rich layer in the rat dentate gyrus following entorhinal lesions. Brain Res. 42, 311–318 (1972)
Lynch, G., Stanfield, B., Cotman, C.W.: Developmental differences in post-lesion axonal growth in the hippocampus. Brain Res. 59, 155–168 (1973)
Nadler, J.V., Cotman, C.W., Lynch, G.S.: Biochemical plasticity of short-axon interneurons: Increased glutamate decarboxylase activity in the denervated area of rat dentate gyrus following entorhinal lesion. Exp. Neurol. 45, 403–413 (1974)
Raisman, G., Cowan, W.M., Powell, T.P.S.: The extrinsic afferent, commissural and association fibers of the hippocampus. Brain 88, 963–996 (1965)
Steward, O., Cotman, C.W., Lynch, G.: Re-establishment of electrophysiologically functional entorhinal cortical input to the dentate gyrus deafferented by ipsilateral entorhinal lesions: Innervation by the contralateral entorhinal cortex. Exp. Brain Res. 18, 396–414 (1973)
Steward, O., Cotman, C.W., Lynch, G.: 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.: Selectivity in the pattern of new synapse formation with denervated dentate granule cells. (abs.) Fourth Annual Meeting of the Society for Neuroscience, St. Louis, Mo. 1974b
Steward, O., Cotman, C.W., 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)
Thomas, R.C., Wilson, V.S.: Precise localization of Renshaw cells with a new marking technique. Nature (Lond.) 206, 211–213 (1965)
White, W.F., Goldowitz, D., Lynch, G., Cotman, C.W.: Electrophysiological analysis of the projection from the contralateral entorhinal cortex to the dentate gyrus in normal rats. Brain Res. 114, 201–209 (1976)
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 (1973)
Zimmer, J.: Long term synaptic reorganization in rat fascia dentata deafferented at adolescent and adult stages: Observations with the Timm method. Brain Res. 76, 336–342 (1974)
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
Some of the material in this paper was included in a dissertation submitted in partial fulfillment of the requirements for the Degree of Doctor of Philosophy at the University of California at Irvine, Irvine, California 92717 (1974).
Rights and permissions
About this article
Cite this article
Steward, O., White, W.F., Cotman, C.W. et al. Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat. Exp Brain Res 26, 423–441 (1976). https://doi.org/10.1007/BF00234223
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00234223