Superior colliculus encodes visual saliency before the primary visual cortex.

Models of visual attention postulate the existence of a bottom-up saliency map that is formed early in the visual processing stream. Although studies have reported evidence of a saliency map in various cortical brain areas, determining the contribution of phylogenetically older pathways is crucial to understanding its origin. Here, we compared saliency coding from neurons in two early gateways into the visual system: the primary visual cortex (V1) and the evolutionarily older superior colliculus (SC). We found that, while the response latency to visual stimulus onset was earlier for V1 neurons than superior colliculus superficial visual-layer neurons (SCs), the saliency representation emerged earlier in SCs than in V1. Because the dominant input to the SCs arises from V1, these relative timings are consistent with the hypothesis that SCs neurons pool the inputs from multiple V1 neurons to form a feature-agnostic saliency map, which may then be relayed to other brain areas.

Superior colliculus neurons encode a visual saliency map during free viewing of natural dynamic video.

Models of visual attention postulate the existence of a saliency map whose function is to guide attention and gaze to the most conspicuous regions in a visual scene. Although cortical representations of saliency have been reported, there is mounting evidence for a subcortical saliency mechanism, which pre-dates the evolution of neocortex. Here, we conduct a strong test of the saliency hypothesis by comparing the output of a well-established computational saliency model with the activation of neurons in the primate superior colliculus (SC), a midbrain structure associated with attention and gaze, while monkeys watched video of natural scenes. We find that the activity of SC superficial visual-layer neurons (SCs), specifically, is well-predicted by the model. This saliency representation is unlikely to be inherited from fronto-parietal cortices, which do not project to SCs, but may be computed in SCs and relayed to other areas via tectothalamic pathways.

Evidence for a link between the experiential allocation of saccade preparation and visuospatial attention.

Whether a link exists between the two orienting processes of saccade preparation and visuospatial attention has typically been studied by using either sensory cues or predetermined rules that instruct subjects where to allocate these limited resources. In the real world, explicit instructions are not always available and presumably expectations shaped by previous experience play an important role in the allocation of these processes. Here we examined whether manipulating two experiential factors that clearly influence saccade preparation--the probability and timing of saccadic responses--also influences the allocation of visuospatial attention. Occasionally, a visual probe was presented whose spatial location and time of presentation varied relative to those of the saccade target. The proportion of erroneous saccades directed toward this probe indexed saccade preparation, and the proportion of correct discriminations of probe orientation indexed visuospatial attention. Overall, preparation and attention were significantly correlated to each other across these manipulations of saccade probability and timing. Saccade probability influenced both preparation and attention processes, whereas saccade timing influenced only preparation processes. Unexpectedly, discrimination ability was not improved in those trials in which the probe triggered an erroneous saccade despite particularly heightened levels of saccade preparation. To account for our results, we propose a conceptual dual-purpose threshold model based on neurophysiological considerations that link the processes of saccade preparation and visuospatial attention. The threshold acts both as the minimum activity level required for eliciting saccades and a maximum level for which neural activity can provide attentional benefits.