Ibotenic acid lesions of the substantia nigra pars reticulata ipsilateral to a visual cortical lesion fail to restore visual orienting responses in the cat.

Unilateral removal of all known visual cortical areas in the cat renders the animal hemianopic in the contralateral visual field as measured by visual perimetry and other behavioral tests. We have shown that visual orientation behavior can be restored to the previously blind hemifield by destruction of a critical zone in the substantia nigra pars reticulata contralateral to a cortical lesion (Wallace et al., J. Comp. Neurol. 296:222-252, 1990). The model proposed to explain this recovery postulates that damage to the crossed nigrotectal projection disinhibits the superior colliculus ipsilateral to the cortical lesion and this leads to recovery. If disinhibition can account for recovery, then destruction of the uncrossed nigrotectal projection, which is known to exert a tonic inhibition on the superior colliculus, should also result in recovery. We made unilateral visual cortical ablations and ipsilateral ibotenic acid lesions of the substantia nigra pars reticulata. Visual orienting behavior was assessed in animals for a period of 4 to 31 weeks. Contrary to the prediction of the model, we failed to observe a recovery of visual orienting behavior in the blind hemifield in any of 23 animals.

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.

Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behavior in the hemianopic cat.

Transection of non-tectotectal fibers in the caudal one-half of the commissure of the superior colliculus restores visual orienting to a cat previously rendered hemianopic by a large unilateral visual cortical lesion. Other observations related to this recovery phenomenon (i.e., the Sprague effect) have suggested that the caudal commissural fibers whose destruction produces the recovery 1) are contralateral afferents to the superior colliculus on the side of the cortical lesion, and 2) profoundly influence visuo-motor processing in this superior colliculus. We performed anatomical and behavioral experiments to determine which of the more than 40 contralateral collicular afferents are directly involved in the Sprague effect. To guide subsequent behavioral studies, we performed a pilot anatomical experiment in which we injected WGA-HRP unilaterally into one superior colliculus at identical retinotopic loci in each of a pair of cats. One cat was normal (control), and the other (experimental) had previously received a caudal transection of the collicular commissure. Quantitative comparison of the retrograde labeling in collicular afferents revealed that a number of mesencephalic regions contain neurons that project to the colliculus via the caudal collicular commissure. Additional collicular injections of WGA-HRP demonstrated the exact location and distribution of collicular afferent neurons within these nuclei. In the behavioral experiments, we attempted to replicate the Sprague effect by destroying the neurons giving rise to the axons in the caudal collicular commissure. Ibotenic acid lesions of these neurons were performed in cats that were hemianopic following the removal of the contralateral visual cortex. Small lesions of a "critical zone" in the rostro-lateral substantia nigra pars reticulata and possibly the overlying ventral zona incerta consistently produced a visual recovery whereas lesions of the other collicular afferents did not. Paradoxically, large nigral lesions that also included the critical zone did not result in a recovery. A conceptual framework for these findings involving striato-nigro-tecto-preoculomotor interactions is presented.

Recovery from cortical blindness mediated by destruction of nontectotectal fibers in the commissure of the superior colliculus in the cat.

Transection of the commissure of the superior colliculus restores visual orientation behavior to a cat previously rendered hemianopic by a unilateral visual cortical lesion (the Sprague effect). Using two methods, we asked whether this recovery resulted from the severing of the tectotectal component of the commissure or whether the destruction of some other connection was responsible. First, we transected either the rostral or the caudal one-half of the tectal commissure in hemianopic cats. If destruction of tectotectal fibers is responsible for the Sprague effect, then only rostral transections should produce the recovery since nearly all tectotectal connections lie in the rostral one-half of the commissure. However, rostral cuts failed to produce a recovery, whereas caudal commisurotomies did. Second, ibotenic acid was used to destroy the cells in the superior colliculus contralateral to the cortical lesion. This lesion eliminated the contralateral tectotectal pathway from the contralateral colliculus but left other fibers (originating elsewhere but coursing through the commissure) largely intact. These ibotenic acid lesions failed to produce the recovery; but when the caudal portion of the tectal commissure was subsequently transected in the same animals, the recovery was observed. The results of both experiments support the conclusion that the transection of a nontectotectal component of the commissure of the superior colliculus is responsible for the recovery of visual orientation behavior in a cortically blind cat.

Localization of a circadian pacemaker in the eye of a mollusc, bulla.

The eye of the marine mollusc Bulla contains a circadian pacemaker which, along with critical entrainment pathways, is located among a small group of neurons at the base of the retina. Long-term intracellular recording from cells of the organized photoreceptor layer, which constitutes most of the retinal volume, indicates that these cells are not involved in generating the rhythm since rhythmic changes in membrane potential were not observed. In addition, surgical removal of the entire photoreceptor layer does not alter the period of the circadian rhythm and does not prevent phase shifts by light pulses.