Role of the Superior Colliculus in Multisensory Orientation Behaviors

The mammalian superior colliculus (SC) has long been known to play a central role in the control of visuomotor behaviors. More recently, the SC has been shown to be important in motor behaviors directed toward auditory and somatosensory stimuli.

As a major site for the convergence and integration of information from these different senses, it has been assumed that the SC plays a critical role in the control of multisensory behaviors as well. This belief has been strongly reinforced by the finding of striking parallels between the activity of multisensory SC neurons and overt behaviors directed toward multisensory stimuli. Thus, stimulus complexes that enhance the activity of multisensory SC neurons also facilitate multisensory-directed behaviors, whereas those that depress the activity of these neurons inhibit behavioral performance.

It has been shown that deactivation of an area of association cortex in the cat (the anterior ectosylvian sulcus or AES) compromises multisensory-mediated behaviors, raising the possibility that these orientation behaviors are mediated by cortical multisensory circuits, rather than by multisensory interactions in the SC.

To directly test the role of the SC in multisensory-mediated behaviors, we carried out excitotoxic lesions of the SC and examined behavioral performance before and after the lesions.

Unilateral SC lesions were found to selectively compromise multisensory (i.e., visual-auditory) enhancements and depressions of response to stimuli in the contralateral hemifield, while modality-specific behaviors (i.e., visual alone) were unaffected by the lesions. Bilateral SC lesions eliminated multisensory enhancements to stimuli at all locations. Taken together, these results establish the central role of the SC in mediating the behavioral enhancements and depressions seen to multisensory stimuli.

Intriguingly, although the elimination of multisensory-mediated behaviors was complete following these lesions, we found that significant portions of the SC were spared from damage. To reconcile this finding with the behavior, we are in the process of recording neuronal responses in the SC of these lesioned cases.