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The Journal of Neuroscience, April 28, 2004, 24(17):4145-4156; doi:10.1523/JNEUROSCI.0199-04.2004

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Behavioral/Systems/Cognitive
Involvement of Monkey Inferior Colliculus in Spatial Hearing

Marcel P. Zwiers,^1,2 Huib Versnel,^1,3 and A. John Van Opstal¹

¹Department of Medical Physics and Biophysics, University of Nijmegen, 6525 EZ Nijmegen, The Netherlands, and ²Structural Neuroimaging Section, Department of Psychiatry and ³Department of Otorhinolaryngology, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands

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.

Key words: inferior colliculus; superior colliculus; monkey; oculomotor; sound; localization

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Received July 11, 2003; revised February 27, 2004; accepted March 5, 2004.

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