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Submillisecond kinetics and low efficacy of parallel fibre-Golgi cell synaptic currents in the rat cerebellum

Stéphane Dieudonné

1. The whole-cell configuration of the patch clamp technique was used to record from Golgi cells in thin slices of the rat cerebellum (P12-P25). Their active membrane properties and the input that they receive from the parallel fibres were characterized.

2. Most cells were filled with biocytin and morphologically identified by the presence of a large axonal arbor restricted to the granular layer. The morphological parameters of eighteen of the best-preserved cells were quantified.

3. A slow capacitive current transient, characteristic of the Golgi cell axon, was used to identify Golgi cells whenever their morphology could not be preserved.

4. Golgi cells fire action potentials spontaneously at 3 ± 1·7 Hz (n = 17). Their firing frequency increases linearly with the amplitude of depolarizing current pulses and displays marked adaptation.

5. When hyperpolarized Golgi cells display an anomalous rectification which is blocked by 2 mM CsCl, indicating the presence of an I_h-like current.

6. Golgi cells receive a spontaneous excitatory input from parallel fibres. This input is composed of small amplitude, mostly monoquantal, EPSCs. Chemical stimulation of granule cells by locally applied kainate evokes tetrodotoxin (TTX)-dependent events with similar properties.

7. The parallel fibre-Golgi cell EPSCs have both AMPA and NMDA components. The NMDA component is blocked by 1 mM external magnesium at -60 mV and decays with time constants of 31 ± 9 ms and 170 ± 15 ms (at +61 mV in the presence of magnesium).

8. In the presence of 10 µM internal spermine, the AMPA component of the spontaneous EPSCs is markedly slowed (0·96 ± 0·25 ms to 1·86 ± 0·47 ms; n = 4) and reduced in amplitude (49 ± 7 %; n = 4) when depolarizing the cell from -70 mV to +61 mV.

9. The decay kinetics of individual AMPA EPSCs were found to be variable, in part because of dendritic filtering. A more detailed analysis reveals that the synaptic AMPA conductances are regulated during development and close faster at days P19-P25 than at days P13-P16.

10. These data suggest that the efficacy of the parallel fibre-Golgi cell input is rather low. This places strong constraints on the conditions in which the inhibitory feedback exerted by the Golgi cell can be operational.

11. The possibility is considered that the Golgi cell-granule cell circuit shows an oscillatory behaviour. This hypothesis is discussed in relation to the models of Albus and Marr.

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