The cerebellar Purkinje cell receives two inputs: a single climbing fibre (CF) and many thousands of parallel fibres (PF). These synapses are each surrounded by a glial sheath, formed from the processes of specialized astrocytes, the Bergmann glial cells. Bergmann glia express Ca²⁺-permeable AMPA receptors and electrogenic glutamate transporters, which evoke inward currents following PF or CF stimulation, providing a pathway for neuron-glial transmission. We previously reported, using whole cell patch clamp recordings in juvenile (16-20 day) rat cerebellar slices, that repetitive stimulation of PFs in the 0.1-1 Hz range depresses this neuron-glial transmission without overt effect on the strength of transmission at adjacent synapses (Bellamy and Ogden, 2006), demonstrating that these ancillary pathways can express plasticity independently of the synaptic network. We have now investigated the specificity of this neuron-glial plasticity. Stimulation of CFs in the 0.1-1 Hz range led to depression of glial currents, in a closely similar manner to that observed at PFs. Depression of the two inputs was independent: either PF or CF inputs could be depressed by raising stimulation frequency from 0.033 to 1 Hz, without affecting the strength of the other input. Furthermore, by stimulation of proximal and distal regions of the molecular layer, we found that separate PFs could be independently depressed, indicating that the decrease in AMPAR and transporter current amplitude was not due to a general desensitization of the glial cell or a change in cable properties. Finally, stimulation of granule neurons in the granular layer rather than molecular layer, so as to activate PF synapses over a distributed area of the Purkinje and Bergmann glial cells, also exhibited depression of glial currents (enhanced by preincubation with 50 μM cyclothiazide), indicating that crosstalk between adjacent PF is not necessary for neuron-glial plasticity. These findings demonstrate specific and dynamic regulation of the strength of neuron to glial signalling at the major synapses in the cerebellum.