The substantia nigra pars reticulata (SNr) is a main output nucleus of the basal ganglia (BG), where inputs from the competing direct and indirect pathways converge onto the same neurons. Interestingly, these inputs are differentially distributed with direct and indirect pathway projections arriving at distal and proximal regions of the dendritic arbor, respectively. We employ a novel method combining theory with electrophysiological experiments and optogenetics to study the distinct effects of inputs arriving at different locations along the dendrite. Our approach represents a useful compromise between complexity and reduction in modelling. Our work addresses the question of high fidelity encoding of inputs by networks of neurons in the new context of pacemaking neurons, which are driven to fire by their intrinsic dynamics rather than by a network state. We provide the first empirical demonstration that dendritic delays can introduce latencies in the responses of a population of neurons that are commensurate with synaptic delays, suggesting a new role for SNr dendrites with implications for BG function.