Superior colliculus lesions preferentially disrupt multisensory orientation

Abstract

The general involvement of the superior colliculus (SC) in orientation behavior and the striking parallels between the multisensory responses of SC neurons and overt orientation behaviors have led to assumptions that these neural and behavioral changes are directly linked. However, deactivation of two areas of cortex which also contain multisensory neurons, the anterior ectosylvian sulcus and rostral lateral suprasylvian sulcus have been shown to eliminate multisensory orientation behaviors, suggesting that this behavior may not involve the SC. To determine whether the SC contributes to this behavior, cats were tested in a multisensory (i.e. visual-auditory) orientation task before and after excitotoxic lesions of the SC. For unilateral SC lesions, modality-specific (i.e. visual or auditory) orientation behaviors had returned to pre-lesion levels after several weeks of recovery. In contrast, the enhancements and depressions in behavior normally seen with multisensory stimuli were severely compromised in the contralesional hemifield. No recovery of these behaviors was observed within the 6 month testing period. Immunohistochemical labeling of the SC revealed a preferential loss of parvalbumin-immunoreactive pyramidal neurons in the intermediate layers, a presumptive multisensory population that targets premotor areas of the brainstem and spinal cord. These results highlight the importance of the SC for multisensory behaviors, and suggest that the multisensory orientation deficits produced by cortical lesions are a result of the loss of cortical influences on multisensory SC neurons.