Transient potentiation of spontaneous EPSPs in rat messy cells induced by depolarization of a single neurone

B. W. Strowbridge, Philip A Schwartzkroin

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1. The amplitude and frequency of spontaneously occurring EPSPs recorded intracellularly in rat messy cells was estimated by measuring membrane potential variance in short segments of a continuous voltage record. Changes in variance reflected changes in the amplitude and/or the frequency of spontaneous EPSPs. 2. Short trains of depolarizing current pulses evoked a delayed increase in membrane potential variance in 55% of trials. Variance increased by 487% during these responses and remained elevated for 124 ± 16 s. Increases in variance were not associated with large changes in the intrinsic properties of the messy cell such as resting membrane potential and input resistance. We termed this phenomenon depolarization-related potentiation (DRP). 3. Epochs of elevated variance were associated with an increase in both the average amplitude and frequency of spontaneous EPSPs. During the peak of the response, the mean interval between spontaneous EPSPs decreased by 36.8%. Computer-generated voltage records with randomly distributed EPSP amplitudes and inter-EPSP intervals suggested that this decrease in inter-EPSP intervals was not sufficient to account for the magnitude of the variance increase observed. Based on this model, we estimated that a 90% increase in the average amplitude of spontaneous EPSPs, in addition to the experimentally measured decrease in the average inter-EPSP interval, was required to reproduce the magnitude of the change in variance observed. In the potentiated state, the amplitude of spontaneous EPSPs often exceeded 10 mV. 4. We also observed epochs of increased variance that occurred spontaneously. These spontaneous epochs closely resembled epochs evoked by depolarizing stimuli, suggesting that the stimulus was acting as a trigger for a spontaneously occurring behaviour. Additional evidence supporting this hypothesis was provided by the observation that stereotyped patterns of increased variance could be evolved by brief stimuli, such as a single 5s depolarizing step. Dual intracellular recordings from two messy cells demonstrated that spontaneous epochs of increased variance occurred independently in different neurones. This result makes it unlikely that these variance increases were due to a global change in the slice environment such as a propagating wave of potassium ions. Bath application of the Na+ channel blocker TTX eliminated most, but not all, of the normal on-going spontaneous EPSPs in messy cells. Treatment with depolarizing current pulses was effective in potentiating TTX-resistant spontaneous EPSPs in three of seven trials. Potentiation also decreased the mean interval between TTX-resistant miniature EPSPs (by an average of 66.9%) in two trials examined. 6. These results suggest that DRP results from the activation of an intrinsic phenomenon within the dentate gyrus by strong depolarization of a single messy cell. Our data suggest that several mechanisms are involved in the expression of DRP since changes in EPSP amplitude and frequency can occur with varying delays from the stimulus. The ability of depolarizing current pulses to potentiate TTX-resistant miniature EPSPs suggests that at least one component of this plasticity occurs at the granule cell-messy cell synapse.

Original languageEnglish (US)
Pages (from-to)493-510
Number of pages18
JournalJournal of Physiology
Issue number2
StatePublished - Jul 15 1996
Externally publishedYes

ASJC Scopus subject areas

  • Physiology


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