TRANSIENT POTENTIATION OF SPONTANEOUS EPSPS IN RAT MOSSY CELLS INDUCED BY DEPOLARIZATION OF A SINGLE NEURON

Citation
Bw. Strowbridge et Pa. Schwartzkroin, TRANSIENT POTENTIATION OF SPONTANEOUS EPSPS IN RAT MOSSY CELLS INDUCED BY DEPOLARIZATION OF A SINGLE NEURON, Journal of physiology, 494(2), 1996, pp. 493-510
Citations number
26
Categorie Soggetti
Physiology
Journal title
ISSN journal
00223751
Volume
494
Issue
2
Year of publication
1996
Pages
493 - 510
Database
ISI
SICI code
0022-3751(1996)494:2<493:TPOSEI>2.0.ZU;2-1
Abstract
1. The amplitude and frequency of spontaneously occurring EPSPs record ed intracellularly in rat messy cells was estimated by measuring membr ane potential variance in short segments of a continuous voltage recor d. Changes in variance reflected changes in the amplitude and/or the f requency 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 rem ained elevated for 124 +/- 16 s. Increases in variance were not associ ated with large changes in the intrinsic properties of the messy cell such as resting membrane potential and input resistance. We termed thi s phenomenon depolarization-related potentiation (DRP). 3. Epochs of e levated variance were associated with an increase in both the average amplitude and frequency of spontaneous EPSPs. During the peak of the r esponse, the mean interval between spontaneous EPSPs decreased by 36.8 %. Computer-generated voltage records with randomly distributed EPSP a mplitudes and inter-EPSP intervals suggested that this decrease in int er-EPSP intervals was not sufficient to account for the magnitude of t he variance increase observed. Based on this model, we estimated that a 90% increase in the average amplitude of spontaneous EPSPs, in addit ion to the experimentally measured decrease in the average inter-EPSP interval, was required to reproduce the magnitude of the change in var iance observed. In the potentiated state, the amplitude of spontaneous EPSPs often exceeded 10 mV. 4. We also observed epochs of increased v ariance that occurred spontaneously These spontaneous epochs closely r esembled epochs evoked by depolarizing stimuli, suggesting that the st imulus was acting as a trigger for a spontaneously occurring behaviour . Additional evidence supporting this hypothesis was provided by the o bservation that stereotyped patterns of increased variance could be ev oked by brief stimuli, such as a single 5 s depolarizing step. Dual in tracellular recordings from two messy cells demonstrated that spontane ous epochs of increased variance occurred independently in different n eurones. This result makes it unlikely that these variance increases w ere due to a global change in the slice environment such as a propagat ing wave of potassium ions. 5. Bath application of the Na+ channel blo cker TTX eliminated most, but not all, of the normal on-going spontane ous EPSPs in messy cells. Treatment with depolarizing current pulses w as 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 activati on of an intrinsic phenomenon within the dentate gyrus by strong depol arization of a single messy cell. Our data suggest that several mechan isms are involved in the expression of DRP since changes in EPSP ampli tude and frequency can occur with varying delays from the stimulus. Th e ability of depolarizing current pulses to potentiate TTX-resistant m iniature EPSPs suggests that at least one component of this plasticity occurs at tile granule cell-messy cell synapse.