Cross-Modal Competition: The Default Computation for Multisensory Processing.

Abstract

Mature multisensory superior colliculus (SC) neurons integrate information across the senses to enhance their responses to spatiotemporally congruent cross-modal stimuli. The development of this neurotypic feature of SC neurons requires experience with cross-modal cues. In the absence of such experience the response of an SC neuron to congruent cross-modal cues is no more robust than its response to the most effective component cue. This "default" or "naive" state is believed to be one in which cross-modal signals do not interact. The present results challenge this characterization by identifying interactions between visual-auditory signals in male and female cats reared without visual-auditory experience. By manipulating the relative effectiveness of the visual and auditory cross-modal cues that were presented to each of these naive neurons, an active competition between cross-modal signals was revealed. Although contrary to current expectations, this result is explained by a neuro-computational model in which the default interaction is mutual inhibition. These findings suggest that multisensory neurons at all maturational stages are capable of some form of multisensory integration, and use experience with cross-modal stimuli to transition from their initial state of competition to their mature state of cooperation. By doing so, they develop the ability to enhance the physiological salience of cross-modal events thereby increasing their impact on the sensorimotor circuitry of the SC, and the likelihood that biologically significant events will elicit SC-mediated overt behaviors.SIGNIFICANCE STATEMENT The present results demonstrate that the default mode of multisensory processing in the superior colliculus is competition, not non-integration as previously characterized. A neuro-computational model explains how these competitive dynamics can be implemented via mutual inhibition, and how this default mode is superseded by the emergence of cooperative interactions during development.