Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus

Abstract

Many neurons in the deeper layers of the superior colliculus (SC) respond to multiple sensory inputs--visual, auditory, and somatic--as well as provide signals essential for saccadic eye movements to targets in different modalities. When the eyes and pinnae are in primary position, the neural map of auditory space is in rough topographic alignment with the map of visual space, and if the auditory map is based solely on headpinna coordinates, any changes in eye position in the orbit will cause misalignment of the maps. We investigated the effects of eye position on the response of sound-sensitive neurons in the SC of cats because previous work on cats and on monkeys had suggested the possibility of species differences in the representation of auditory signals in the SC. We also investigated the effects of eye position on the accuracy of saccades to auditory, visual, and bimodal stimuli. All studies were conducted in alert, trained cats with the head restrained in a fixed position. Neuronal and behavioral responses were studied during periods when the eyes were steadily directed to different positions relative to the position of the sound. Cats showed partial compensation for eye position in making saccades, regardless of the modality of the target, and they showed similar patterns of error in saccades to auditory and visual targets. These behavioral data are consistent with coding the location of visual and auditory targets in the same coordinate system. In the vast majority of intermediate-layer neurons, eye position significantly affected the number of spikes evoked by sound stimuli. For most of these neurons, changes in eye position produced significant shifts in the speaker location producing maximal response. In some neurons, eye position significantly facilitated the magnitude of neuronal response evoked by sounds from a variety of speaker locations. Because few pinna movements could be detected, in is unlikely that these changes in neuronal response could be due to changes in the position of the pinnae. Our results indicate that the deep layers of the SC contain an eye-centered representation of sound location. Because eye position did not affect the percentage of neurons exhibiting multimodal integration, visual and auditory maps appear to remain integrated in the SC even when the eyes are directed eccentrically.(ABSTRACT TRUNCATED AT 400 WORDS)