Neurons in the inferior olive and cerebellum are important for motor coordination. While global deletion of HCN1 channels impairs coordinated motor behaviours, the mechanisms involved are not known. In particular, the roles of HCN1 channels expressed by specific cell types in the inferior olive and cerebellum are not well understood. To address this issue we have adopted a combination of electrophysiological, genetic and behavioural approaches. We find distinct cellular functions for HCN1 channels expressed by three key cell types in the olivo-cerebellar circuit. In Purkinje cells, HCN1 channels stabilize the relationship between input and output, without affecting spontaneous firing. By contrast, in cerebellar basket cells, HCN1 channels suppress the emergence of slow oscillatory activity, while in the inferior olive HCN1 channels paradoxically suppress excitability by maintaining neurons in a depolarized state. To begin to investigate how HCN1 channels in each cell type influence motor behaviour, we have generated mice with deletion of HCN1 channels restricted to cerebellar Purkinje cells. We find that this deletion reproduces in part motor behaviour deficits found in mice with global deletion of HCN1 channels, suggesting specific behavioural roles for HCN1 channels expressed by cerebellar Purkinje cells. Together our data demonstrate that the functional roles of HCN1 channels depend on the cellular context in which they are expressed and point towards cell type specific roles of HCN1 channels in motor behaviour.