Abstract

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.

Highlights

  • 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

  • We hypothesize that visual saliency is coded in the primate superior colliculus (SC) (Fig. 1b) because: (1) it is heavily interconnected with early visual areas[20]; (2) it encodes stimuli in a featureless manner[21,22,23]; (3) it has a well-defined topography[24]; and (4) it has long-range centre-surround organization well suited for a saliency mechanism[25]

  • To test the hypothesis that SCs represents a visual saliency map, three rhesus monkeys freely viewed a series of high-definition video clips of natural dynamic scenes while we recorded extracellular activity of single SC neurons (Fig. 2a)

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Summary

Introduction

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. Empirical and computational modelling studies have reported evidence of a saliency and/or priority map in various cortical brain areas (for example, V1 (refs 5–7); V4 (refs 8,9); lateral intraparietal area, LIP10–12; frontal eye fields, FEF13; dorsolateral prefrontal cortex[14]) While these studies used intuitive definitions of saliency with simple stimuli under restricted viewing conditions, a strong test of the saliency hypothesis would be to use a well-established computational model to correlate neuronal firing rates with model-predicted saliency during unconstrained viewing of natural dynamic scenes. We hypothesize that visual saliency is poorly represented in the SCi because activation of these neurons is highly dependent upon goal-directed attention and gaze behaviour[26,27,28,29], owing to its dominant inputs from frontal/parietal areas and basal ganglia, and its direct output to the brainstem saccade circuit[30] This has led to the hypothesis that SCi best represents a behavioural priority map[4]

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