Involvement of monkey inferior colliculus in spatial hearing

The midbrain inferior colliculus (IC) is implicated in coding sound location, but evidence from behaving primates is scarce. Here we report single-unit responses to broadband sounds that were systematically varied within the two-dimensional (2D) frontal hemifield, as well as in sound level, while monkeys fixated a central visual target. Results show that IC neurons are broadly tuned to both sound-source azimuth and level in a way that can be approximated by multiplicative, planar modulation of the firing rate of the cell. In addition, a fraction of neurons also responded to elevation. This tuning, however, was more varied: some neurons were sensitive to a specific elevation; others responded to elevation in a monotonic way. Multiple-linear regression parameters varied from cell to cell, but the only topography encountered was a dorsoventral tonotopy. In a second experiment, we presented sounds from straight ahead while monkeys fixated visual targets at different positions. We found that auditory responses in a fraction of IC cells were weakly, but systematically, modulated by 2D eye position. This modulation was absent in the spontaneous firing rates, again suggesting a multiplicative interaction of acoustic and eye-position inputs. Tuning parameters to sound frequency, location, intensity, and eye position were uncorrelated. On the basis of simulations with a simple neural network model, we suggest that the population of IC cells could encode the head-centered 2D sound location and enable a direct transformation of this signal into the eye-centered topographic motor map of the superior colliculus. Both signals are required to generate rapid eye-head orienting movements toward sounds.