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 t...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 114; no. 35; pp. 9451 - 9456
Main Authors White, Brian J., Kan, Janis Y., Levy, Ron, Itti, Laurent, Munoz, Douglas P.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 29.08.2017
Subjects
Animals
Attention
Attention - physiology
Biological Sciences
Brain
Brain mapping
Information processing
Latency
Macaca mulatta
Male
Neural coding
Neurons
Neurons - physiology
Photic Stimulation
Phylogeny
Psychophysics
Reaction Time
Social Sciences
Studies
Superior Colliculi
Superior colliculus
Visual cortex
Visual Cortex - physiology
Visual Pathways - physiology
Visual perception
Visual stimuli
Visual system
vision
attention
priority
gaze
oculomotor
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Summary: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.
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Edited by Marlene Cohen, University of Pittsburgh, Pittsburgh, PA and accepted by Editorial Board Member Marlene Behrmann July 18, 2017 (received for review January 18, 2017)
Author contributions: B.J.W., J.Y.K., L.I., and D.P.M. designed research; B.J.W. and J.Y.K. performed research; R.L. contributed new reagents/analytic tools; B.J.W. and J.Y.K. analyzed data; R.L. was the primary surgeon in the chronic implantation of a microelectrode array in the primary visual cortex; L.I. contributed significantly to the research idea and hypotheses and cowrote portions of the manuscript; and B.J.W., J.Y.K., and D.P.M. wrote the paper.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1701003114