Auditory receptive fields in primate superior colliculus shift with changes in eye position

Abstract

The process by which sensory signals are transformed into commands for the control of movement is poorly understood. A potential site for such a transformation is the superior colliculus (SC), which receives auditory, visual and somatosensory inputs^1–3 and contains neurones that discharge before saccadic eye movements^4–6. Along the primary sensory pathways, signals coding the spatial location of auditory, visual and somatosensory targets are based on distinctly different coordinate systems, and it is not known whether each type of sensory input uses a separate motor pathway or if they are converted into a common coordinate system in order to share a single pre-motor circuit. Sensory neurones in the SC have spatially restricted receptive fields (RFs) and are organized into maps across the collicular surface^7–9. Acute experiments have shown a rough correspondence between the spatial positions of RFs of neurones encountered along a single dorsal–ventral penetration of the colliculus, regardless of the modality of the effective stimulus^10–14, suggesting that auditory, visual and somatosensory maps might be in register. However, in these conditions the head-centred auditory system and the retinotopic visual system are aligned because the eyes are in the primary orbital position¹⁵. Moreover, other data have suggested^16–18 that the primate SC is organized in motor, not sensory, coordinates, although in the cat, eye position was found to have no effect on auditory receptive fields¹⁹. We therefore sought here to determine what happens to the registration of the auditory and visual maps in the alert, behaving animal. Monkeys, with heads fixed, were trained to make delayed saccadic eye movements to auditory or visual targets from one of three initial fixation points while the activity of single neurones was recorded extracellularly. We found that the auditory receptive fields shifted with changes in eye position, allowing the auditory and visual maps to remain in register.