Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo

The cutaneous parallel fiber (PF) receptive fields of cerebellar stellate and basket cells in the cerebellar C3 zone in vivo are normally very small but can be dramatically enlarged by climbing fiber (CF)-dependent plasticity. To analyze the effects of this receptive field plasticity, we present for the first time whole-cell patch-clamp recordings from these interneurons during natural and electrical activation of cutaneously driven synaptic input. In “naive” interneurons, peripheral input nearly exclusively activated a few (two to eight) large PF EPSPs from a specific small skin area that overlapped the receptive field of the local CF input. After conjunctive PF and CF stimulation, numerous small and large EPSPs and ramp-like depolarizations could be activated from the entire forelimb skin. These findings therefore confirm previous suggestions that conjunctive PF and CF activation leads to a long-lasting potentiation of PF synaptic input to interneurons. The CF response, which is crucial for the induction of the PF synaptic potentiation, was strong but variable and very different from the conventional EPSPs evoked by PFs.