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The Journal of Neuroscience, February 15, 2000, 20(4):1348-1357

Modulation of Transmission during Trains at a Cerebellar Synapse

Anatol C. Kreitzer and Wade G. Regehr

Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115

Activity-dependent processes dynamically regulate synapses on the time scale of milliseconds to seconds. Here, we examine the factors governing synaptic strength during repetitive stimulation, both in control conditions and during presynaptic inhibition. Field recordings of presynaptic volleys, optical measurements of presynaptic calcium, and voltage-clamp recordings of postsynaptic currents were used to examine parallel fiber to Purkinje cell synapses in cerebellar brain slices at 34°C. In control conditions, regular stimulus trains (1-50 Hz) evoked up to a 250% peak synaptic enhancement, whereas during irregular stimulation, a threefold variability in EPSC amplitude was observed. When initial EPSC amplitudes were reduced by 50%, either by lowering external calcium or by activating adenosine A₁ or GABA_B receptors, the peak enhancement during regular trains was 500%, and synaptic variability during irregular trains was nearly sixfold. By contrast, changes in fiber excitability and calcium influx per pulse were small during trains. Presynaptic calcium measurements indicated that by pulse 10, stimulus-evoked calcium influx had increased by ~15%, which on the basis of the measured relationship between calcium influx and release corresponds to an EPSC enhancement of 50%. This enhancement was the same in all experimental conditions, even in the presence of N⁶-cyclopentyladenosine or baclofen, suggesting that repetitive stimulation does not relieve the G-protein inhibition of calcium channels by these modulators. Therefore, for our experimental conditions, changes in synaptic strength during trains are primarily attributable to residual calcium (Ca_res)-dependent short-term plasticities, and the actions of neuromodulators during repetitive stimulation result from their inhibition of initial calcium influx and the resulting effects on Ca_res and calcium-driven processes.

Key words: GABA_B receptor; adenosine A₁ receptor; presynaptic inhibition; short-term plasticity; residual calcium; cerebellar granule cell; cerebellar Purkinje cell

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Copyright © 2000 Society for Neuroscience  0270-6474/00/2041348-10$05.00/0

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