Elsevier

Neuroscience

Volume 124, Issue 3, 2004, Pages 535-547
Neuroscience

Superior colliculus lesions preferentially disrupt multisensory orientation

https://doi.org/10.1016/j.neuroscience.2003.12.026Get rights and content

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.

Section snippets

General description

All experimental procedures were conducted using aseptic techniques and were in accordance with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health Publication 86-23) and an approved Wake Forest University School of Medicine Animal Care and Use Committee protocol and all efforts were made to minimize the number of animals used. Using standard shaping methods, cats (n=7) were trained with food rewards to orient to either visual or auditory stimuli presented within

Pre-lesion behavior

In the six animals trained to orient to visual stimuli (five with unilateral lesions and one with a bilateral lesion), pre-lesion data were consistent with previous reports examining multisensory orientation behaviors (Stein et al., 1988, Stein et al., 1989, Wilkinson et al., 1996, Jiang et al., 2002). Thus, when an unrewarded (i.e. neutral) auditory stimulus was combined with a visual stimulus at the same location (spatially coincident trials), there was a significant increase in the

Discussion

The results of the current study demonstrate that the integrity of the SC is essential to maintain an animal's ability to integrate visual and auditory cues in the control of orientation behavior. Excitotoxic lesions of the multisensory layers of the SC eliminated this ability, thereby rendering a stimulus from one modality (e.g. auditory) incapable of modulating the salience of a target stimulus from another modality (e.g. visual). This result is consistent with earlier suggestions regarding

Acknowledgements

We would like to acknowledge Dr. John McHaffie for his assistance with the histology, and Dr. Craig Henkel for his assistance with the cell count analysis. This work was supported by NIH MH63861, NS22543 and NS36916.

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