Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina

Summary: An antagonistic center-surround receptive field is a key feature in sensory processing, but how it contributes to specific computations such as direction selectivity is often unknown. Retinal On-starburst amacrine cells (SACs), which mediate direction selectivity in direction-selective gang...

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Main Authors: Lea Ankri, Elishai Ezra-Tsur, Shir R. Maimon, Nathali Kaushansky, Michal Rivlin-Etzion
Format: Article
Language:English
Published: Elsevier 2020-05-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S221112472030557X
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author Lea Ankri
Elishai Ezra-Tsur
Shir R. Maimon
Nathali Kaushansky
Michal Rivlin-Etzion
author_facet Lea Ankri
Elishai Ezra-Tsur
Shir R. Maimon
Nathali Kaushansky
Michal Rivlin-Etzion
author_sort Lea Ankri
collection DOAJ
description Summary: An antagonistic center-surround receptive field is a key feature in sensory processing, but how it contributes to specific computations such as direction selectivity is often unknown. Retinal On-starburst amacrine cells (SACs), which mediate direction selectivity in direction-selective ganglion cells (DSGCs), exhibit antagonistic receptive field organization: depolarizing to light increments and decrements in their center and surround, respectively. We find that a repetitive stimulation exhausts SAC center and enhances its surround and use it to study how center-surround responses contribute to direction selectivity. Center, but not surround, activation induces direction-selective responses in SACs. Nevertheless, both SAC center and surround elicited direction-selective responses in DSGCs, but to opposite directions. Physiological and modeling data suggest that the opposing direction selectivity can result from inverted temporal balance between excitation and inhibition in DSGCs, implying that SAC’s response timing dictates direction selectivity. Our findings reveal antagonistic center-surround mechanisms for direction selectivity and demonstrate how context-dependent receptive field reorganization enables flexible computations.
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spelling doaj.art-07201b11295242b7aa0539998f6b6ac02022-12-22T00:07:09ZengElsevierCell Reports2211-12472020-05-01315Antagonistic Center-Surround Mechanisms for Direction Selectivity in the RetinaLea Ankri0Elishai Ezra-Tsur1Shir R. Maimon2Nathali Kaushansky3Michal Rivlin-Etzion4Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, IsraelDepartment of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel; Department of Mathematics and Computer Science, The Open University of Israel, Ra’anana, IsraelDepartment of Neurobiology, Weizmann Institute of Science, Rehovot 76100, IsraelDepartment of Neurobiology, Weizmann Institute of Science, Rehovot 76100, IsraelDepartment of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel; Corresponding authorSummary: An antagonistic center-surround receptive field is a key feature in sensory processing, but how it contributes to specific computations such as direction selectivity is often unknown. Retinal On-starburst amacrine cells (SACs), which mediate direction selectivity in direction-selective ganglion cells (DSGCs), exhibit antagonistic receptive field organization: depolarizing to light increments and decrements in their center and surround, respectively. We find that a repetitive stimulation exhausts SAC center and enhances its surround and use it to study how center-surround responses contribute to direction selectivity. Center, but not surround, activation induces direction-selective responses in SACs. Nevertheless, both SAC center and surround elicited direction-selective responses in DSGCs, but to opposite directions. Physiological and modeling data suggest that the opposing direction selectivity can result from inverted temporal balance between excitation and inhibition in DSGCs, implying that SAC’s response timing dictates direction selectivity. Our findings reveal antagonistic center-surround mechanisms for direction selectivity and demonstrate how context-dependent receptive field reorganization enables flexible computations.http://www.sciencedirect.com/science/article/pii/S221112472030557Xneural circuitsneural computationvisual processingretinaantagonistic center-surroundreceptive field
spellingShingle Lea Ankri
Elishai Ezra-Tsur
Shir R. Maimon
Nathali Kaushansky
Michal Rivlin-Etzion
Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
Cell Reports
neural circuits
neural computation
visual processing
retina
antagonistic center-surround
receptive field
title Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
title_full Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
title_fullStr Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
title_full_unstemmed Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
title_short Antagonistic Center-Surround Mechanisms for Direction Selectivity in the Retina
title_sort antagonistic center surround mechanisms for direction selectivity in the retina
topic neural circuits
neural computation
visual processing
retina
antagonistic center-surround
receptive field
url http://www.sciencedirect.com/science/article/pii/S221112472030557X
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AT elishaiezratsur antagonisticcentersurroundmechanismsfordirectionselectivityintheretina
AT shirrmaimon antagonisticcentersurroundmechanismsfordirectionselectivityintheretina
AT nathalikaushansky antagonisticcentersurroundmechanismsfordirectionselectivityintheretina
AT michalrivlinetzion antagonisticcentersurroundmechanismsfordirectionselectivityintheretina