The identification and characterization of organization principals is essential for the understanding of neural function of brain areas. The inferior colliculus (IC) represents a midbrain nexus involved in numerous aspects of auditory processing. Likewise, neurons throughout the IC are tuned to a diverse range of specific stimulus features. Yet beyond a topographic arrangement of the cochlea-inherited frequency tuning, the functional organization of the IC is not well understood. Particularly, a common principle that links the diverse tuning characteristics is unknown. Here we used in vitro patch clamp recordings combined with laser-uncaging, and in vivo single cell recordings to study the spatial and functional organization principles of the central IC. We identified a topographic bias of ascending synaptic input timing that is balanced between inhibition and excitation and co-varies with in vivo first–spike latency. This bias was paralleled post-synaptically by differences in biophysical membrane properties and firing patterns, with integrating neurons predominantly found in the dorso-medial part, and coincidence-detector neurons biased to the ventro-lateral IC. Importantly, these cellular and network features translated into distinct temporal processing capabilities irrespectively of the neurons' characteristic frequency. Our data therefore imply that heterogeneity of synaptic inputs, intrinsic properties and temporal processing are functional principles that underlie the spatial organization of the central IC.