Using superior colliculus principles of multisensory integration to reverse hemianopia

Abstract

The diversity of our senses conveys many advantages; it enables them to compensate for one another when needed, and the information they provide about a common event can be integrated to facilitate its processing and, ultimately, adaptive responses. These cooperative interactions are produced by multisensory neurons. A well-studied model in this context is the multisensory neuron in the output layers of the superior colliculus (SC). These neurons integrate and amplify their cross-modal (e.g., visual-auditory) inputs, thereby enhancing the physiological salience of the initiating event and the probability that it will elicit SC-mediated detection, localization, and orientation behavior. Repeated experience with the same visual-auditory stimulus can also increase the neuron's sensitivity to these individual inputs. This observation raised the possibility that such plasticity could be engaged to restore visual responsiveness when compromised. For example, unilateral lesions of visual cortex compromise the visual responsiveness of neurons in the multisensory output layers of the ipsilesional SC and produces profound contralesional blindness (hemianopia). The possibility that multisensory plasticity could restore the visual responses of these neurons, and reverse blindness, was tested in the cat model of hemianopia. Hemianopic subjects were repeatedly presented with spatiotemporally congruent visual-auditory stimulus pairs in the blinded hemifield on a daily or weekly basis. After several weeks of this multisensory exposure paradigm, visual responsiveness was restored in SC neurons and behavioral responses were elicited by visual stimuli in the previously blind hemifield. The constraints on the effectiveness of this procedure proved to be the same as those constraining SC multisensory plasticity: whereas repetitions of a congruent visual-auditory stimulus was highly effective, neither exposure to its individual component stimuli, nor to these stimuli in non-congruent configurations was effective. The restored visual responsiveness proved to be robust, highly competitive with that in the intact hemifield, and sufficient to support visual discrimination.