Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration

Abstract

Convergence of inputs from different sensory modalities onto individual neurons is a phenomenon that occurs widely throughout the brain at many phyletic levels and appears to represent a basic neural mechanism by which an organism integrates complex environmental stimuli. In the present study, neurons in the superior colliculus (SC) were used as a model to examine how single neurons deal with simultaneous cues from different sensory modalities (e.g., visual, auditory, somatosensory). The functional result of multisensory convergence on an individual cell was determined by comparing the responses evoked from it by a combined-modality (multimodal) stimulus with those elicited by each (unimodal) component of that stimulus presented alone. Superior colliculus cells exhibited profound changes in their activity when individual sensory stimuli were combined. These "multisensory interactions" were found to be widespread among deep laminae cells and fell into one of two functional categories: response enhancement, characterized by a significant increase in the number of discharges evoked; and response depression, characterized by a significant decrease in the discharges elicited. Multisensory response interactions most often reflected a multiplicative, rather than summative, change in activity. Their absolute magnitude varied from cell to cell and, when stimulus conditions were altered, within the same cell. However, the percentage change of enhanced interactions was generally inversely related to the vigor of the responses that could be evoked by presenting each unimodal stimulus alone and suggest that the potential for response amplification was greatest when responses evoked by individual stimuli were weakest. The majority of cells exhibiting multi-sensory characteristics were demonstrated to have descending efferent projections and thus had access to premotor and motor areas of the brain stem and spinal cord involved in SC-mediated attentive and orientation behaviors. These data show that multisensory convergence provides the descending efferent cells of the SC with a dynamic response character. The responses of these cells and the SC-mediated behaviors that they underlie need not be immutably tied to the presence of any single stimulus, but can vary in response to the particular complex of stimuli present in the environment at any given moment.