Ibotenic acid lesions in the pedunculopontine region result in recovery of visual orienting in the hemianopic cat.

Cats rendered hemianopic by a unilateral visual cortical ablation can recover the visual orienting response in the hemianopic visual field following disruption of the caudal non-tectotectal containing half of the commissure of the superior colliculus. Ibotenic acid lesions of a small 'critical zone' in the contralateral substantia nigra result in a similar recovery effect. A conceptual framework developed by Wallace et al. (1990) [J. Comp. Neurol. 296, 222-252] proposed that elimination of contralateral substantia nigra 'critical zone' inhibition on the superior colliculus ipsilateral to a visual cortical lesion is responsible for the recovery. This model is insufficient, however, to explain the observation that hemi-decorticate cats with contralateral substantia nigra 'critical zone' lesions which include but extend beyond the 'critical zone' do not demonstrate the recovery. In these cats, subsequent transection of the commissure of the superior colliculus does lead to the recovery. We hypothesize that another projection through the caudal commissure of the superior colliculus, from the pedunculopontine nucleus, is involved in the recovery effect. Visual orienting behavior was recorded before and after ibotenic acid lesions made in the pedunculopontine nucleus region contralateral to a visual cortical ablation in 16 cats. Four cats with lesions in a small rostral region of the contralateral pedunculopontine nucleus recovered the visual orienting response in the previously hemianopic visual field. Contralateral tectal projections from the pedunculopontine nucleus are thought to be cholinergic and terminate as distinct patches in the intermediate gray layers of the superior colliculus. Since this region of the pedunculopontine nucleus also receives GABA-ergic afferents from the substantia nigra, we propose that a subcortical neural circuit including the substantia nigra, pedunculopontine nucleus, and superior colliculus is involved in the recovery of visual orienting.

Ibotenic acid lesions of the superior colliculus produce longer lasting deficits in visual orienting behavior than aspiration lesions in the cat.

We compared the effects of unilateral surgical aspiration and ibotenic acid produced lesions of the superior colliculus (SC) on visual orienting behavior in 20 cats. Four animals with aspiration lesions initially showed an hemianopia in the contralateral hemifield which recovered fully in 4.5 weeks or less. These lesions also destroyed axons in the commissure of the superior colliculus (CS). In 9 animals we produced complete loss of cells in one SC, with preservation of axons in the CSC, by injections of ibotenic acid. In these animals the contralateral hemianopia persisted for an average of 16.6 weeks, but may have persisted longer had we not intervened by either sacrificing the animal or ablating the visual cortex contralateral to the SC lesion. The cortical lesion produced an immediate hemianopia in the contralateral hemifield and a recovery in the previously hemianopic ('collicular') hemifield. In the remaining 7 animals with attempted ibotenic acid lesions, 5 had incomplete lesions and 2 others sustained major damage to the SC as well as the CSC. These 7 animals recovered visual orienting on an average of 3.0 weeks postoperatively. We conclude that unilateral loss of collicular cell function and the presence of fibers coursing through the commissure of the superior colliculus are both necessary for the prolonged deficit in visual orienting behavior. We suggest that competition between the two hemifields may play a role in the hemianopia caused by collicular manipulations and that the cholinergic pathway from the pedunculopontine nucleus to the contralateral SC via the CSC may be involved.