Multisensory Versus Unisensory Integration: Contrasting Modes in the Superior Colliculus

Abstract

The present study suggests that the neural computations used to integrate information from different senses are distinct from those used to integrate information from within the same sense. Using superior colliculus neurons as a model, it was found that multisensory integration of cross-modal stimulus combinations yielded responses that were significantly greater than those evoked by the best component stimulus. In contrast, unisensory integration of within-modal stimulus pairs yielded responses that were similar to or less than those evoked by the best component stimulus. This difference is exemplified by the disproportionate representations of superadditive responses during multisensory integration and the predominance of subadditive responses during unisensory integration. These observations suggest that different rules have evolved for integrating sensory information, one (unisensory) reflecting the inherent characteristics of the individual sense and, the other (multisensory), unique supramodal characteristics designed to enhance the salience of the initiating event.

A neural network model of multisensory integration also accounts for unisensory integration in superior colliculus

“…These tests consisted of interleaved trials in which the two visual stimuli (V 1 and V 2 ) were presented within the neuron's receptive field individually and in combination, and at 3 levels of effectiveness. As shown previously, responses to within-modal stimuli did not significantly exceed those to the most effective of the component stimuli at any effectiveness level (Alvarado et al, 2007a;2007b). This result is in marked contrast to the response enhancement typically observed when visual and non-visual stimuli (cross-modal) are combined (e.g., see Meredith and Stein, 1986;Kadunce et al, 1997;Stein 1998;Wallace et al, 1998;Jiang et al, 2001;Perrault et al, 2003;Stanford et al, 2005) and speaks to differences in the mechanisms underlying multisensory and unisensory integration.…”

“…Because unisensory visual integration takes place in both multisensory and unisensory neurons (Alvarado et al, 2007a;2007b), both were included in this sample population (multisensory: n = 87 [55%]; unisensory: n = 71 [45%]). Figure 2 shows the results of within-modal tests in a typical multisensory neuron.…”

“…In order to evaluate the accuracy of the neural network model in describing the products of unisensory integration, its predictions were compared to those of three other computational models (maximum operator, averaging, and additive) used previously to analyze these data (Alvarado et al, 2007a(Alvarado et al, , 2007b. The neural network model predicts that the response to two modality-specific stimuli will be determined by Eq.…”

“…2; that is, it will reflect a nonlinear combination of the responses evoked by either stimulus individually. The additive model predicts that the response to two stimuli will be equivalent to the sum of the responses evoked by the stimuli individually (Stanford et al, 2005;Alvarado et al, 2007aAlvarado et al, ,2007b). The averaging model predicts that the response to two stimuli will be equivalent to the mean of the responses evoked by the stimuli individually (Heeger, 1992;Rolls and Tovee, 1995;Carandini et al, 1997;Recanzone et al, 1997;Britten and Heuer, 1999;Reynolds et al, 1999;Treue et al, 2000;Heuer and Britten, 2002;Zoccolan et al, 2005).…”

“…Consequently, the model predicts that the response to multiple within-modal stimuli should be similar to either the average or maximum of the single-stimulus responses. A series of recent physiological studies by Alvarado et al, (2007aAlvarado et al, ( , 2007b explored the unisensory integrative capabilities of multisensory SC neurons using multiple visual stimuli. Here we evaluate the accuracy of the neural network model in predicting those data.…”