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Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation
Despite their small size, microsaccades can impede stimulus detections if executed at inopportune times. Although it has been shown that microsaccades evoke both inhibitory and excitatory responses across different visual regions, their impact on the higher-level neural decision processes that bridg...
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Published in: | The Journal of neuroscience 2018-02, Vol.38 (9), p.2163-2176 |
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description | Despite their small size, microsaccades can impede stimulus detections if executed at inopportune times. Although it has been shown that microsaccades evoke both inhibitory and excitatory responses across different visual regions, their impact on the higher-level neural decision processes that bridge sensory responses to action selection has yet to be examined. Here, we show that when human observers monitor stimuli for subtle feature changes, the occurrence of microsaccades long after (up to 800 ms) change onset predicts slower reaction times and this is accounted for by momentary suppression of neural signals at each key stage of decision formation: visual evidence encoding, evidence accumulation, and motor preparation. Our data further reveal that, independent of the timing of the change events, the onset of neural decision formation coincides with a systematic inhibition of microsaccade production, persisting until the perceptual report is executed. Our combined behavioral and neural measures highlight antagonistic interactions between microsaccade occurrence and evidence accumulation during visual decision-making tasks.
When fixating on a location in space, we frequently make tiny eye movements called microsaccades. In the present study, we show that these microsaccades impede our ability to make perceptual decisions about visual stimuli and this impediment specifically occurs via the disruption of several processing levels of the sensorimotor network: the encoding of visual evidence itself, the accumulation of visual evidence toward a response, and effector-selective motor preparation. Furthermore, we show that the production of microsaccades is inhibited during the perceptual decision, possibly as a counteractive measure to mitigate their negative effect on behavior in this context. The combined behavioral and neural measures used in this study provide strong and novel evidence for the interaction of fixational eye movements and the perceptual decision-making process. |
doi_str_mv | 10.1523/JNEUROSCI.2340-17.2018 |
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When fixating on a location in space, we frequently make tiny eye movements called microsaccades. In the present study, we show that these microsaccades impede our ability to make perceptual decisions about visual stimuli and this impediment specifically occurs via the disruption of several processing levels of the sensorimotor network: the encoding of visual evidence itself, the accumulation of visual evidence toward a response, and effector-selective motor preparation. Furthermore, we show that the production of microsaccades is inhibited during the perceptual decision, possibly as a counteractive measure to mitigate their negative effect on behavior in this context. The combined behavioral and neural measures used in this study provide strong and novel evidence for the interaction of fixational eye movements and the perceptual decision-making process.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.2340-17.2018</identifier><identifier>PMID: 29371320</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Accumulation ; Adult ; Coding ; Decision making ; Decision Making - physiology ; Eye ; Eye movements ; Female ; Humans ; Male ; Motors ; Reaction Time - physiology ; Saccades - physiology ; Sensorimotor system ; Visual Perception - physiology ; Visual signals ; Visual stimuli ; Visual tasks</subject><ispartof>The Journal of neuroscience, 2018-02, Vol.38 (9), p.2163-2176</ispartof><rights>Copyright © 2018 the authors 0270-6474/18/382163-14$15.00/0.</rights><rights>Copyright Society for Neuroscience Feb 28, 2018</rights><rights>Copyright © 2018 the authors 0270-6474/18/382163-14$15.00/0 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-4ae1537ee22b0bb8c070cc30ade46b82965574c7ebff59f450503c0b060782f83</citedby><cites>FETCH-LOGICAL-c442t-4ae1537ee22b0bb8c070cc30ade46b82965574c7ebff59f450503c0b060782f83</cites><orcidid>0000-0001-8240-1876 ; 0000-0003-1961-5294</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596275/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596275/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29371320$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Loughnane, Gerard M</creatorcontrib><creatorcontrib>Newman, Daniel P</creatorcontrib><creatorcontrib>Tamang, Sarita</creatorcontrib><creatorcontrib>Kelly, Simon P</creatorcontrib><creatorcontrib>O'Connell, Redmond G</creatorcontrib><title>Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Despite their small size, microsaccades can impede stimulus detections if executed at inopportune times. Although it has been shown that microsaccades evoke both inhibitory and excitatory responses across different visual regions, their impact on the higher-level neural decision processes that bridge sensory responses to action selection has yet to be examined. Here, we show that when human observers monitor stimuli for subtle feature changes, the occurrence of microsaccades long after (up to 800 ms) change onset predicts slower reaction times and this is accounted for by momentary suppression of neural signals at each key stage of decision formation: visual evidence encoding, evidence accumulation, and motor preparation. Our data further reveal that, independent of the timing of the change events, the onset of neural decision formation coincides with a systematic inhibition of microsaccade production, persisting until the perceptual report is executed. Our combined behavioral and neural measures highlight antagonistic interactions between microsaccade occurrence and evidence accumulation during visual decision-making tasks.
When fixating on a location in space, we frequently make tiny eye movements called microsaccades. In the present study, we show that these microsaccades impede our ability to make perceptual decisions about visual stimuli and this impediment specifically occurs via the disruption of several processing levels of the sensorimotor network: the encoding of visual evidence itself, the accumulation of visual evidence toward a response, and effector-selective motor preparation. Furthermore, we show that the production of microsaccades is inhibited during the perceptual decision, possibly as a counteractive measure to mitigate their negative effect on behavior in this context. The combined behavioral and neural measures used in this study provide strong and novel evidence for the interaction of fixational eye movements and the perceptual decision-making process.</description><subject>Accumulation</subject><subject>Adult</subject><subject>Coding</subject><subject>Decision making</subject><subject>Decision Making - physiology</subject><subject>Eye</subject><subject>Eye movements</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Motors</subject><subject>Reaction Time - physiology</subject><subject>Saccades - physiology</subject><subject>Sensorimotor system</subject><subject>Visual Perception - physiology</subject><subject>Visual signals</subject><subject>Visual stimuli</subject><subject>Visual tasks</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNpdUctu1DAUtRCIDoVfqCKxYZPp9StONkjDdEoHFYqAri3HczO4SuzWTor4exxaRsDqLs5D555DyAmFJZWMn374tLn-cvV1vV0yLqCkasmA1k_IIqNNyQTQp2QBTEFZCSWOyIuUbgBAAVXPyRFruKKcwYIMKz-affAujc4WWz9iNHZ0wafiHY4_EH3x0dkYkrHW7DAVxu-Kzb3bobdYrKydhqk3s6D4HIPFlDLnbIrO74sztC7NyHmIw2_OS_KsM33CV4_3mFyfb76tL8rLq_fb9eqytEKwsRQGqeQKkbEW2ra2Obe1HHIAUbU1ayoplbAK266TTSckSOAWWqhA1ayr-TF5--B7O7UD7iz6MZpe30Y3mPhTB-P0v4h33_U-3OtKNhVTMhu8eTSI4W7CNOrBJYt9bzyGKWnaNLlvySqaqa__o96EKfr8nmbQCFHXks2JqgfW3GWK2B3CUNDzovqwqJ4X1VTpedEsPPn7lYPsz4T8F8ipn6I</recordid><startdate>20180228</startdate><enddate>20180228</enddate><creator>Loughnane, Gerard M</creator><creator>Newman, Daniel P</creator><creator>Tamang, Sarita</creator><creator>Kelly, Simon P</creator><creator>O'Connell, Redmond G</creator><general>Society for Neuroscience</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8240-1876</orcidid><orcidid>https://orcid.org/0000-0003-1961-5294</orcidid></search><sort><creationdate>20180228</creationdate><title>Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation</title><author>Loughnane, Gerard M ; Newman, Daniel P ; Tamang, Sarita ; Kelly, Simon P ; O'Connell, Redmond G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-4ae1537ee22b0bb8c070cc30ade46b82965574c7ebff59f450503c0b060782f83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Accumulation</topic><topic>Adult</topic><topic>Coding</topic><topic>Decision making</topic><topic>Decision Making - physiology</topic><topic>Eye</topic><topic>Eye movements</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Motors</topic><topic>Reaction Time - physiology</topic><topic>Saccades - physiology</topic><topic>Sensorimotor system</topic><topic>Visual Perception - physiology</topic><topic>Visual signals</topic><topic>Visual stimuli</topic><topic>Visual tasks</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Loughnane, Gerard M</creatorcontrib><creatorcontrib>Newman, Daniel P</creatorcontrib><creatorcontrib>Tamang, Sarita</creatorcontrib><creatorcontrib>Kelly, Simon P</creatorcontrib><creatorcontrib>O'Connell, Redmond G</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Loughnane, Gerard M</au><au>Newman, Daniel P</au><au>Tamang, Sarita</au><au>Kelly, Simon P</au><au>O'Connell, Redmond G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2018-02-28</date><risdate>2018</risdate><volume>38</volume><issue>9</issue><spage>2163</spage><epage>2176</epage><pages>2163-2176</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Despite their small size, microsaccades can impede stimulus detections if executed at inopportune times. Although it has been shown that microsaccades evoke both inhibitory and excitatory responses across different visual regions, their impact on the higher-level neural decision processes that bridge sensory responses to action selection has yet to be examined. Here, we show that when human observers monitor stimuli for subtle feature changes, the occurrence of microsaccades long after (up to 800 ms) change onset predicts slower reaction times and this is accounted for by momentary suppression of neural signals at each key stage of decision formation: visual evidence encoding, evidence accumulation, and motor preparation. Our data further reveal that, independent of the timing of the change events, the onset of neural decision formation coincides with a systematic inhibition of microsaccade production, persisting until the perceptual report is executed. Our combined behavioral and neural measures highlight antagonistic interactions between microsaccade occurrence and evidence accumulation during visual decision-making tasks.
When fixating on a location in space, we frequently make tiny eye movements called microsaccades. In the present study, we show that these microsaccades impede our ability to make perceptual decisions about visual stimuli and this impediment specifically occurs via the disruption of several processing levels of the sensorimotor network: the encoding of visual evidence itself, the accumulation of visual evidence toward a response, and effector-selective motor preparation. Furthermore, we show that the production of microsaccades is inhibited during the perceptual decision, possibly as a counteractive measure to mitigate their negative effect on behavior in this context. The combined behavioral and neural measures used in this study provide strong and novel evidence for the interaction of fixational eye movements and the perceptual decision-making process.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>29371320</pmid><doi>10.1523/JNEUROSCI.2340-17.2018</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8240-1876</orcidid><orcidid>https://orcid.org/0000-0003-1961-5294</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Accumulation Adult Coding Decision making Decision Making - physiology Eye Eye movements Female Humans Male Motors Reaction Time - physiology Saccades - physiology Sensorimotor system Visual Perception - physiology Visual signals Visual stimuli Visual tasks |
title | Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation |
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