Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys

Visual objects are recognized by their features. Whereas, some features are based on simple components (i.e., local features, such as orientation of line segments), some features are based on the whole object (i.e., global features, such as an object having a hole in it). Over the past five decades,...

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Main Authors: Jun Huang, Yan Yang, Ke Zhou, Xudong Zhao, Quan Zhou, Hong Zhu, Yingshan Yang, Chunming Zhang, Yifeng Zhou, Wu Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fnins.2017.00474/full
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author Jun Huang
Jun Huang
Yan Yang
Ke Zhou
Ke Zhou
Ke Zhou
Xudong Zhao
Quan Zhou
Hong Zhu
Hong Zhu
Hong Zhu
Yingshan Yang
Chunming Zhang
Yifeng Zhou
Yifeng Zhou
Wu Zhou
Wu Zhou
Wu Zhou
spellingShingle Jun Huang
Jun Huang
Yan Yang
Ke Zhou
Ke Zhou
Ke Zhou
Xudong Zhao
Quan Zhou
Hong Zhu
Hong Zhu
Hong Zhu
Yingshan Yang
Chunming Zhang
Yifeng Zhou
Yifeng Zhou
Wu Zhou
Wu Zhou
Wu Zhou
Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
Frontiers in Neuroscience
topological perception
visual search
feature integration
saccade
behaving monkeys
author_facet Jun Huang
Jun Huang
Yan Yang
Ke Zhou
Ke Zhou
Ke Zhou
Xudong Zhao
Quan Zhou
Hong Zhu
Hong Zhu
Hong Zhu
Yingshan Yang
Chunming Zhang
Yifeng Zhou
Yifeng Zhou
Wu Zhou
Wu Zhou
Wu Zhou
author_sort Jun Huang
title Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
title_short Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
title_full Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
title_fullStr Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
title_full_unstemmed Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving Monkeys
title_sort rapid processing of a global feature in the on visual pathways of behaving monkeys
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2017-08-01
description Visual objects are recognized by their features. Whereas, some features are based on simple components (i.e., local features, such as orientation of line segments), some features are based on the whole object (i.e., global features, such as an object having a hole in it). Over the past five decades, behavioral, physiological, anatomical, and computational studies have established a general model of vision, which starts from extracting local features in the lower visual pathways followed by a feature integration process that extracts global features in the higher visual pathways. This local-to-global model is successful in providing a unified account for a vast sets of perception experiments, but it fails to account for a set of experiments showing human visual systems' superior sensitivity to global features. Understanding the neural mechanisms underlying the “global-first” process will offer critical insights into new models of vision. The goal of the present study was to establish a non-human primate model of rapid processing of global features for elucidating the neural mechanisms underlying differential processing of global and local features. Monkeys were trained to make a saccade to a target in the black background, which was different from the distractors (white circle) in color (e.g., red circle target), local features (e.g., white square target), a global feature (e.g., white ring with a hole target) or their combinations (e.g., red square target). Contrary to the predictions of the prevailing local-to-global model, we found that (1) detecting a distinction or a change in the global feature was faster than detecting a distinction or a change in color or local features; (2) detecting a distinction in color was facilitated by a distinction in the global feature, but not in the local features; and (3) detecting the hole was interfered by the local features of the hole (e.g., white ring with a squared hole). These results suggest that monkey ON visual systems have a subsystem that is more sensitive to distinctions in the global feature than local features. They also provide the behavioral constraints for identifying the underlying neural substrates.
topic topological perception
visual search
feature integration
saccade
behaving monkeys
url http://journal.frontiersin.org/article/10.3389/fnins.2017.00474/full
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spelling doaj-5e57d9388ba64dad96f69db429ef15382020-11-24T22:39:46ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2017-08-011110.3389/fnins.2017.00474270677Rapid Processing of a Global Feature in the ON Visual Pathways of Behaving MonkeysJun Huang0Jun Huang1Yan Yang2Ke Zhou3Ke Zhou4Ke Zhou5Xudong Zhao6Quan Zhou7Hong Zhu8Hong Zhu9Hong Zhu10Yingshan Yang11Chunming Zhang12Yifeng Zhou13Yifeng Zhou14Wu Zhou15Wu Zhou16Wu Zhou17CAS Key Laboratory of Brain Function and Disease, and School of Life Sciences, University of Science and Technology of ChinaHefei, ChinaDepartment of Otolaryngology and Communicative Sciences, University of Mississippi Medical CenterJackson, MS, United StatesState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of SciencesBeijing, ChinaCollege of Psychology and Sociology, Shenzhen UniversityShenzhen, ChinaCenter for Language and Brain, Shenzhen Institute of NeuroscienceShenzhen, ChinaShenzhen Key Laboratory of Affective and Social Cognitive Science, Shenzhen UniversityShenzhen, ChinaState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of SciencesBeijing, ChinaState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of SciencesBeijing, ChinaDepartment of Otolaryngology and Communicative Sciences, University of Mississippi Medical CenterJackson, MS, United StatesDepartment of Neurobiology and Anatomical Sciences, University of Mississippi Medical CenterJackson, MS, United StatesDepartment of Neurology, University of Mississippi Medical CenterJackson, MS, United StatesPrimate Research Center of Jin Gang InternationalHaikou, China0Department of Otolaryngology, First Affiliated Hospital, Shanxi Medical UniversityTaiyuan, ChinaCAS Key Laboratory of Brain Function and Disease, and School of Life Sciences, University of Science and Technology of ChinaHefei, ChinaState Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of SciencesBeijing, ChinaDepartment of Otolaryngology and Communicative Sciences, University of Mississippi Medical CenterJackson, MS, United StatesDepartment of Neurobiology and Anatomical Sciences, University of Mississippi Medical CenterJackson, MS, United StatesDepartment of Neurology, University of Mississippi Medical CenterJackson, MS, United StatesVisual objects are recognized by their features. Whereas, some features are based on simple components (i.e., local features, such as orientation of line segments), some features are based on the whole object (i.e., global features, such as an object having a hole in it). Over the past five decades, behavioral, physiological, anatomical, and computational studies have established a general model of vision, which starts from extracting local features in the lower visual pathways followed by a feature integration process that extracts global features in the higher visual pathways. This local-to-global model is successful in providing a unified account for a vast sets of perception experiments, but it fails to account for a set of experiments showing human visual systems' superior sensitivity to global features. Understanding the neural mechanisms underlying the “global-first” process will offer critical insights into new models of vision. The goal of the present study was to establish a non-human primate model of rapid processing of global features for elucidating the neural mechanisms underlying differential processing of global and local features. Monkeys were trained to make a saccade to a target in the black background, which was different from the distractors (white circle) in color (e.g., red circle target), local features (e.g., white square target), a global feature (e.g., white ring with a hole target) or their combinations (e.g., red square target). Contrary to the predictions of the prevailing local-to-global model, we found that (1) detecting a distinction or a change in the global feature was faster than detecting a distinction or a change in color or local features; (2) detecting a distinction in color was facilitated by a distinction in the global feature, but not in the local features; and (3) detecting the hole was interfered by the local features of the hole (e.g., white ring with a squared hole). These results suggest that monkey ON visual systems have a subsystem that is more sensitive to distinctions in the global feature than local features. They also provide the behavioral constraints for identifying the underlying neural substrates.http://journal.frontiersin.org/article/10.3389/fnins.2017.00474/fulltopological perceptionvisual searchfeature integrationsaccadebehaving monkeys