Encoding of Concurrent Sounds in the Monkey Inferior Colliculus

Abstract

The inferior colliculus (IC) is an auditory midbrain nucleus essential to the perception of sound frequency and the localization of sound source; yet it remains unclear how the firing rate of primate IC neurons contribute to the localization of concurrent sounds of variable sound frequencies. In this work, I extracellularly recorded the activity of 105 IC neurons while two adult macaque monkeys reported the location(s) of either a single bandpass filtered sound or two concurrent bandpass filtered sounds spatially separated by 24° and separated in sound frequency by 0.25 - 2 octaves. Monkeys performed this task well, with an accuracy of about 80% on single sound trials and about 90% on dual sound trials. The improvement in performance on dual sound trials was not explained by dual sound modulations of IC neural response functions. On dual sound trials, IC neuron receptive fields broadened, and sound frequency accounted for less variance in the dual sound response; and these changes decreased the performance of a maximum-likelihood decoder in correctly labeling the condition of a held out dual sound trial by about 20%. Overall, these results suggest that changes to the IC neural response functions elicited by the presence of a second, concurrent, sound should impair rather than facilitate the IC encoding of concurrent sounds and that an alternative explanation is required to account for monkey performance. I next investigated if recently discovered response alternations, suggested to underlie the encoding of concurrent sounds, were present in the recorded populations. These response alternations occur when an IC neuron alternates its firing rate between the rate corresponding to each component sound of a dual sound pair. These response alternations were observed in about 60% of IC neurons and their contribution to the population response remained stable across the full, 2 octave, range of frequency separations tested. Thus, response alternations are a general mechanism used by the IC to potentially facilitate the encoding of multiple sounds and these results add to a growing body of work observing response alternations across brain areas. The measurements I performed clearly indicate that neurons in the primate IC are sensitive to not only sound frequency and location but also the number of sounds in the environment. Future empirical and theoretical work is needed to elucidate how exactly these response alternations arise and are read out by downstream neurons to allow for the perception of concurrent sounds.