Multisensory integration for orienting responses in humans requires the activation of the superior colliculus

Abstract

Animal studies have shown that the superior colliculus (SC) is important for synthesising information from multiple senses into a unified map of space. Here, we tested whether the SC is a critical neural substrate for multisensory spatial integration in humans. To do so, we took advantage of neurophysiological findings revealing that the SC does not receive direct projections from short-wavelength-sensitive S cones. In a simple reaction-time task, participants responded more quickly to concurrent peripheral (extra-foveal) audiovisual (AV) stimuli than to an auditory or visual stimulus alone, a phenomenon known as the redundant target effect (RTE). We show that the nature of this RTE was dependent on the colour of the visual stimulus. When using purple short-wavelength stimuli, to which the SC is blind, RTE was simply explained by probability summation, indicating that the redundant auditory and visual channels are independent. Conversely, with red long-wavelength stimuli, visible to the SC, the RTE was related to nonlinear neural summation, which constitutes evidence of integration of different sensory information. We also demonstrate that when AV stimuli were presented at fixation, so that the spatial orienting component of the task was reduced, neural summation was possible regardless of stimulus colour. Together, these findings provide support for a pivotal role of the SC in mediating multisensory spatial integration in humans, when behaviour involves spatial orienting responses.

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

“…Another possibility is that the differing products of multisensory and unisensory integration properly reflect the pooling of information from two independent sources in the former, and the covariance between information sources in the latter. In either case, these data speak to an important caveat in the interpretation of multisensory enhancements as being produced by a "redundant targets effect" (e.g., Miller, 1982;Gondan et al, 2005;Leo et al, 2007;Lippert et al, 2007;Sinnett et al, 2008), as redundant targets from the same sensory modality do not yield equivalent enhancements either physiologically or behaviorally.…”

Linguistic synaesthesia, perceptual synaesthesia, and the interaction between multiple sensory modalities

“…Interestingly, psychophysical interactions between vision and audition are not present in experimental paradigms involving colours (cf. Leo et al 2008;Arieh and Marks 2008). Figure 5 shows that in synaesthetic pairings between auditory nouns and visual adjectives, eighty percent are constituted by auditory nouns modified by visual adjectives referring to brightness (see examples 4-5), whereas only ten percent are constituted by auditory nouns modified by visual adjectives referring to colour, 29 e.g.,:…”

Audio-Visual Stimulation Improves Visual Search Abilities in Hemianopia due to Childhood Acquired Brain Lesions

“…Furthermore, they provided evidence that audiovisual train ing, presumably by SC stimulation, may induce more organized patterns of visual exploration due to an implementation of efficient oculomotor strategies. Leo et al (2008a) have demonstrated that SC is the critical neural substrate for multisensory spatial integration in humans thanks to an experiment in which participants responded to peripheral (extra-foveal) audiovisual stimuli more quickly than to an auditory or visual stimulus alone -the so-called 'redun dant target effect (RTE)'. This was true only when the colour of the stimulus was red and not purple.…”