Experience is required to develop visual-nonvisual multisensory integration capabilities

Using the multisensory neuron in the cat superior colliculus (SC) as a model, we found that the brain develops its ability to integrate visual and non-visual (auditory and/or somatosensory) stimuli during early postnatal life based on experience with specific cross-modal combinations. For example, precluding visual-auditory experience by rearing animals in darkness or omnidirectional masking broadband sound blocks the maturation of visual-auditory integration capabilities. Individual SC multisensory neurons fail to show their characteristic ability to synthesize inputs from congruent visual-auditory cues and thereby enhance their responses. Animals also fail to show normal multisensory performance benefits in a variety of visual-auditory behavioral tasks, retaining the neonatal or “default” computation whereby these sensory inputs inhibit one another in competing for access to the sensorimotor circuitry of the SC. This condition is only modestly ameliorated when such animals are exposed to a normal environment as adults, suggesting that the mature brain becomes less capable of extracting key cross-modal statistics from normal experience. However, the defect can be overcome via special multisensory “training” paradigms in which spatiotemporally congruent visual-auditory stimulus pairs are regularly and repeatedly presented at a single location in space. With this exposure, visual-auditory SC neurons whose receptive fields encroach on the exposure location change their multisensory computation from competition to one in which congruent visual-auditory stimuli elicit the enhanced responses typical of the normal brain. These physiological changes are paralleled by changes in behavior: after multisensory training, the detection and localization of congruent visual-auditory pairs are now greatly enhanced at the exposure location. These findings reinforce that multisensory experience is crucial for multisensory development at all ages, and that multisensory training can greatly accelerate this development in adult animals relative to the uncontrolled multisensory experience offered by normal environments.