The inferior colliculus (IC) is a well-established target of descending projections from the auditory cortex (AC). However, our understanding of these pathways has been limited by an incomplete picture of their functional influence within the three-dimensional space of the IC. Our goal was to study the properties and spatial representation of corticofugal input in the IC of guinea pigs with a high degree of spatial resolution. We systematically mapped neural activity in the IC using two types of silicon substrate probes that allow for simultaneous recording at multiple neural sites. One probe provided a high resolution in the dorsal-ventral plane and the other provided spatial resolution in the medial-lateral plane. Electrical stimulation of the ipsilateral AC produced excitatory responses in the IC with thresholds usually below 5-10 microA. First spike latencies were predominantly in the 6-20 ms range, although latencies from 3-5 ms were also observed. Broadly distributed unimodal spike patterns with modal latencies greater than 30 ms were occasionally seen. The excitatory responses to cortical stimulation were mostly unimodal and occasionally bimodal with a wide range of spike distribution patterns and response durations. Excitation was often followed by suppression of spontaneous activity. Suppression of acoustic responses was observed even when there was little or no response to electrical stimulation, suggesting spatial-temporal integration. A few of the responding neurons showed purely inhibitory responses to electrical stimulation, suggesting that there are disynaptic routes of corticocollicular inhibition. Detailed spatial mapping revealed that the response patterns and their durations had a characteristic spatial distribution in the IC.