Restoration of Acoustic Orienting Into a Cortically Deaf Hemifield by Reversible Deactivation of the Contralesional Superior Colliculus: The Acoustic “Sprague Effect”

Abstract

Removal of all contiguous visual cortical areas of one hemisphere results in a contralateral hemianopia. Subsequent deactivation of the contralesional superior colliculus (SC) nullifies the effects of the visual cortex ablation and restores visual orienting responses into the cortically blind hemifield. This deficit nullification has become known as the "Sprague Effect." Similarly, in the auditory system, unilateral ablation of auditory cortex results in severe sound localization deficits, as assessed by acoustic orienting, to stimuli in the contralateral hemifield. The purpose of this study was to examine whether auditory orienting responses can be restored into the impaired hemifield during deactivation of the contralesional SC. Three mature cats were trained to orient toward and approach an acoustic stimulus (broadband, white noise burst) that was presented centrally, or at one of 12 peripheral loci, spaced at 15 degrees intervals. After training, a cryoloop was chronically implanted over the dorsal surface of the right SC. During cooling of the cooling loop to temperatures sufficient to deactivate the superficial and intermediate layers (SZ, SGS, SO, SGI), auditory orienting responses were eliminated into the left (contracooled) hemifield while leaving acoustic orienting into the right (ipsicooled) hemifield unimpaired. This deficit was temperature-dependently graded from periphery to center. After the effectiveness of the SC cooling loop was verified, auditory cortex of the middle and posterior ectosylvian and anterior and posterior sylvian gyri was removed from the left hemisphere. As expected, the auditory cortex ablation resulted in a profound deficit in orienting to acoustic stimuli presented at any position in the right (contralesional) hemifield, while leaving acoustic orienting into the left (ipsilesional) hemifield unimpaired. The ablations of auditory cortex did not have any impact on a visual detection and orienting task. The additional deactivation of the contralesional SC to temperatures sufficient to cool the superficial and intermediate layers nullified the deficit caused by the auditory cortex ablation and acoustic orienting responses were restored into the right hemifield. This restoration was temperature-dependently graded from center to periphery. The deactivations were localized and confirmed with reduced uptake of radiolabeled 2-deoxyglucose. Therefore deactivation of the right superior colliculus after the ablation of the left auditory cortex yields a fundamentally different result from that identified during deactivation of the right superior colliculus before the removal of left auditory cortex in the same animal. Thus the "Sprague Effect" is not unique to a particular sensory system and deactivation of the contralesional SC can restore either visual or acoustic orienting responses into an impaired hemifield after cortical damage.