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An evaluation of the synapse specificity of long-term depression induced in rat cerebellar slices

T. Reynolds and N. A. Hartell

1. Whole-cell excitatory postsynaptic currents (EPSCs) were recorded from single Purkinje cells (PCs) in rat cerebellar slices in response to alternate activation of two separate sets of parallel fibres (PF₁ and PF₂). Pairing the stimulation of one input (PF₁) with PC depolarisation at 1 Hz for 5 min produced varied effects, including a long-term depression (LTD) of subsequent responses, a medium-term potentiation, or no change relative to baseline levels (n = 14). In all but two cases PF₂ responses mirrored those in PF₁, in both direction and magnitude even though this second pathway was not specifically activated during pairing.

2. Increasing the stimulus strength to evoke larger amplitude EPSCs (> 1000 pA) dramatically increased the proportion of cells that underwent LTD in both PF₁ and PF₂. LTD in both pathways was postsynaptic calcium dependent. PC depolarisation alone (n = 7) or PF₁ stimulation paired with PC hyperpolarisation (n = 6) failed to induce LTD at either site.

3. Pairing PF₁ stimulation with climbing fibre (CF) activation at 1 Hz for 5 min produced LTD in the majority of cells regardless of the strength of PF stimulation. LTD under these conditions was not, however, input specific, even at the lowest stimulus strengths.

4. With EPSCs greater than 1000 pA in amplitude, depression was apparent in both pathways even when the duration of PF₁ pairing with depolarisation was limited to 1 min. Full expression of LTD in PF₂ required stimulation of this pathway to be resumed within a distinct temporal window of conjunctive pairing with PF₁. Introducing a delay of 20 min before resumption of PF₂ activation preserved the input specificity of synaptic depression.

5. We conclude that pairing either PC depolarisation or CF activation with stimulation of a discrete set of PFs produces LTD that spreads to adjacent synapses on the same PC.

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