The inferior colliculus (IC) can be divided into three anatomical subdivisions: the central nucleus (ICc), the dorsal cortex (ICd) and the external cortex (ICx). ICx receives its primary auditory inputs from ICc and auditory cerebral cortical areas, and non-auditory inputs from regions of motor and other sensory systems. This wide array of projections makes the ICx a distinct structure within the auditory brainstem. The purpose of the current study was to comprehensively characterize the neuronal population of ICx, by intrinsic and synaptic response properties. Visual whole-cell patch clamp recordings were taken from ICx neurons (N=129) from rats between postnatal days 8 to 12. Neurons displayed various types of firing patterns in response to current injection, including regular, adapting, pauser and bursting. The regular cells constitute the majority (66%), followed by adapting (18%), pauser (13%) and bursting cells (2%). In response to hyperpolarizing current injection, many neurons illustrated a pronounced sag in the membrane potential, representing a hyperpolarization-activated current (I(h)). Some neurons (25%) displayed a Ca(2+)-dependent rebound depolarization following negative current injection. In response to depolarizing current injection, 70% of ICx neurons displayed a Ca(2+)-mediated potential expressed as Ca(2+) spikes/humps, uncovered when Na(+) and K(+) currents were removed. Also, spikes displayed an undershoot which was in part mediated by Ca(2+). Stimulation of the ICc elicited graded synaptic responses, which displayed a combination of excitatory and/or inhibitory potentials, with excitation being predominant across firing patterns. Neurons displayed temporal summation in response to repetitive stimulation at 20 Hz and higher. The results indicate a relatively modest diversity in firing pattern and in intrinsic membrane properties, making this subnucleus distinct from its counterparts within the IC. The data show that ICx receives major excitatory input from ICc, supporting its role in integrating signals from brainstem and directing information to higher brain centers.