We compared membrane and synaptic properties of neurons in the three major subdivisions of inferior colliculus (IC), central nucleus (ICc, N=18), external cortex (ICx, N=38), and dorsal cortex (ICd, N=31) of slices from rat IC, using intracellular neuronal recording. Three types of responses occurred in each IC subdivision in response to depolarizing currents: on-type (N=20), rapidly-adapting (N=11), and sustained firing (N=56), which was most common. The on-type neurons have lower input resistances and shorter time constants, with wider and lower amplitude action potentials (APs) than sustained neurons. A calcium-mediated 'hump' was often evoked by depolarizing current pulses in ICd neurons (11 of 28), was infrequent in ICx, but was absent in ICc. ICx and ICc neurons often exhibited spontaneous repetitive spike firing, lower repetitive AP firing thresholds, and faster repetitive spike firing than ICd neurons. Calcium-mediated fast after-hyperpolarizations and spike frequency adaptation were regularly seen in IC. Neurons in ICx and ICd, but not ICc, had synaptic responses to stimulation of the collicular commissure (CoIC). In ICx, large epileptiform depolarizing events were often elicited by strong electrical stimulation of CoIC, which was not normally seen in ICd. These results indicate that ICx neurons exhibit a greater degree of synaptic excitability than neurons in ICc or ICd, which may contribute to the proposed role of ICx in pathological IC hyperexcitability.