Distribution of cortical neurons projecting to the superior colliculus in macaque monkeys

Abstract

To better reveal the pattern of corticotectal projections to the superficial layers of the superior colliculus (SC), we made a total of ten retrograde tracer injections into the SC of three macaque monkeys (Macaca mulatta). The majority of these injections were in the superficial layers of the SC, which process visual information. To isolate inputs to the purely visual layers in the superficial SC from those inputs to the motor and multisensory layers deeper in the SC, two injections were placed to include the intermediate and deep layers of the SC. In another case, an injection was placed in the medial pulvinar, a nucleus not known to be strongly connected with visual cortex, to identify possible projections from tracer spread past the lateral boundary of the SC. Four conclusions are supported by the results: 1) all early visual areas of cortex, including V1, V2, V3, and the middle temporal area, project to the superficial layers of the SC; 2) with the possible exception of the frontal eye field, few areas of cortex outside of the early visual areas project to the superficial SC, although many do, however, project to the intermediate and deep layers of the SC; 3) roughly matching retinotopy is conserved in the projections of visual areas to the SC; and 4) the projections from different visual areas are similarly dense, although projections from early visual areas appear somewhat denser than those of higher order visual areas in macaque cortex.

Superior colliculus encodes visual saliency before the primary visual cortex

“…Moreover, the saliency representation was generally limited to the superficial visual SC layers. SCi visuomotor neurons, with dominant inputs that arise from frontal-parietal cortices and the basal ganglia (23)(24)(25), did not show a significant preference for the salient oddball (Fig. 4 A and B).…”

“…The input-output structure and response characteristics of SCi neurons differ in many important ways from SCs neurons (23)(24)(25). In particular, SCi neurons receive a diverse set of inputs predominantly from frontal and parietal cortices and the basal ganglia (Fig.…”

“…In particular, SCi neurons receive a diverse set of inputs predominantly from frontal and parietal cortices and the basal ganglia (Fig. 1B) and project directly to the brainstem saccade generator (23)(24)(25). Functionally, these neurons have multisensory and oculomotor responses and have been shown to play a central role in spatial attention (19,20).…”

“…Recently (26), it has been shown that the activity of SCs neurons, with dominant inputs that arise from the retina and V1 (Fig. 1B) (24,25), is well-predicted by a computational saliency model that has been validated on the free viewing behavior of humans (27) and nonhuman primates (28). In addition, a recent lesion study has shown that attention guidance is preserved in the absence of V1 (29), thereby challenging the hypothesis that saliency coding depends critically on V1 (6-9) and instead, implicating a possible pathway through the SC.…”

“…1B) is multilayered but is often described as having two dominant functional layers, a superior colliculus superficial layer (SCs) associated exclusively with visual processing and a superior colliculus multisensory-cognitive-motor intermediate layer (SCi) linked to the control of attention and gaze (19)(20)(21)(22). Because SCs is interconnected with multiple visual areas (23)(24)(25), it is in an ideal location to pool diverse visual inputs to form a feature-agnostic saliency representation. Recently (26), it has been shown that the activity of SCs neurons, with dominant inputs that arise from the retina and V1 (Fig.…”