We provide evidence that the brain may use time division multiplexing, or interleaving of different signals across time, to represent multiple items in a single neural channel. We evaluated single unit activity in an auditory coding "bottleneck", the inferior colliculus, while monkeys reported the location(s) of one or two simultaneous sounds. Using novel statistical methods to evaluate spiking activity on a variety of time scales, we found that on dual-sound trials, neurons sometimes alternated between firing rates similar to those observed for each single sound. These fluctuations could occur either across or within trials and appeared coordinated across pairs of simultaneously recorded neurons. Fluctuations could be predicted by the state of local field potentials prior to sound onset, and, in one monkey, predicted which sound the monkey would ultimately saccade to first. Alternation between activity patterns corresponding to each of multiple items may be a general strategy employed by the brain to enhance its processing capacity, suggesting a potential connection between such disparate phenomena as variable neural firing, neural oscillations, and limits in attentional or memory capacity.