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

Abstract

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.

On imputing function to structure from the behavioural effects of brain lesions

“…We note that these uncertainties about double dissociation would not have been emphasized without the startling and paradoxical e¡ects of multiple inactivations, made apparent by careful studies of this system (e.g. Sprague 1966;Lomber & Payne 1996;Wallace et al 1989Wallace et al , 1990.…”

Attention to One or Two Features in Left or Right Visual Field: A Positron Emission Tomography Study

“…These lesion data and the current findings require us to postulate a model in which covert orienting results from the balance among inhibitory, disinhibitory, and facilitatory influences within a distributed attentional system, including the lateral frontal cortex. The complex interplay among different components of such a system may be reminiscent of much better known oculomotor (Wallace et al, 1989(Wallace et al, , 1990) and motor systems (Alexander et al, 1986). Within such a model the absolute sign of the frontal blood flow difference is hard to interpret and may reflect inhibitory, disinhibitory, and facilitatory influences.…”

Topographic Organization of Excitatory and Inhibitory Commissural Connections in the Superior Colliculi and Their Functional Roles in Saccade Generation

“…Many anatomical and behavioral studies on the collicular commissural connections have been devoted to showing the neural mechanism of the Sprague effect (Stein and Meredith 1993). However, more recent studies have shown that this effect is mediated by a pathway other than intrinsic collicular commissural neurons (CNs), because transection of the rostral commissure in the SC, where fibers of the intrinsic collicular CNs are known to run, produced no effect, whereas transection of the caudal commissure produced the Sprague effect (Wallace et al 1989(Wallace et al , 1990.…”