Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat

Abstract

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.