Relatively little is known about how electrically coupled interneuron networks respond to excitatory synaptic input. Cerebellar Golgi cells are an attractive system to study electrical signalling because they do not form reciprocal chemical synaptic connections. Using paired whole-cell recordings from acute slices of mouse cerebellum, we show that gap junction-mediated potentials have a largely inhibitory effect on neighbouring Golgi cells. This ‘electrical inhibition’ is due to the propagation of afterhyperpolarising potentials through connexion-36 gap junctions located on dendrites. Neighbouring Golgi cells tended to synchronize their activity under quiescent conditions. However, stimulation of excitatory mossy fibre input triggered different behaviours in directly innervated Golgi cells and those that did not receive an input. Moreover, when the excitatory input occurred out-of-phase with the intrinsic firing, antiphase firing was triggered. Biologically detailed network models closely reproduced the experimental results and predict that sparse synaptic excitation causes a transient desynchronization of spiking across the network. Our results suggest that several features of sensory-evoked behaviour in the cerebellar granule cell layer could arise from synaptic excitation of the electrically coupled Golgi cell network.