Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT
When processing sensory signals, the brain must account for noise, both noise in the stimulus and that arising from within its own neuronal circuitry. Dopamine receptor activation is known to enhance both visual cortical signal-to-noise-ratio (SNR) and visual perceptual performance; however, it is u...
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description | When processing sensory signals, the brain must account for noise, both noise in the stimulus and that arising from within its own neuronal circuitry. Dopamine receptor activation is known to enhance both visual cortical signal-to-noise-ratio (SNR) and visual perceptual performance; however, it is unknown whether these two dopamine-mediated phenomena are linked. To assess this, we used single-pulse transcranial magnetic stimulation (TMS) applied to visual cortical area V5/MT to reduce the SNR focally and thus disrupt visual motion discrimination performance to visual targets located in the same retinotopic space. The hypothesis that dopamine receptor activation enhances perceptual performance by improving cortical SNR predicts that dopamine activation should antagonize TMS disruption of visual perception. We assessed this hypothesis via a double-blinded, placebo-controlled study with the dopamine receptor agonists cabergoline (a D2 agonist) and pergolide (a D1/D2 agonist) administered in separate sessions (separated by 2 weeks) in 12 healthy volunteers in a William's balance-order design. TMS degraded visual motion perception when the evoked phosphene and the visual stimulus overlapped in time and space in the placebo and cabergoline conditions, but not in the pergolide condition. This suggests that dopamine D1 or combined D1 and D2 receptor activation enhances cortical SNR to boost perceptual performance. That local visual cortical excitability was unchanged across drug conditions suggests the involvement of long-range intracortical interactions in this D1 effect. Because increased internal noise (and thus lower SNR) can impair visual perceptual learning, improving visual cortical SNR via D1/D2 agonist therapy may be useful in boosting rehabilitation programs involving visual perceptual training.
In this study, we address the issue of whether dopamine activation improves visual perception despite increasing sensory noise in the visual cortex. We show specifically that dopamine D1 (or combined D1/D2) receptor activation enhances the cortical signal-to-noise-ratio to boost perceptual performance. Together with the previously reported effects of dopamine upon brain plasticity and learning (Wolf et al., 2003; Hansen and Manahan-Vaughan, 2014), our results suggest that combining rehabilitation with dopamine agonists could enhance both the saliency of the training signal and the long-term effects on brain plasticity to boost rehabilitation regimens for brain in |
doi_str_mv | 10.1523/jneurosci.4452-15.2016 |
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In this study, we address the issue of whether dopamine activation improves visual perception despite increasing sensory noise in the visual cortex. We show specifically that dopamine D1 (or combined D1/D2) receptor activation enhances the cortical signal-to-noise-ratio to boost perceptual performance. Together with the previously reported effects of dopamine upon brain plasticity and learning (Wolf et al., 2003; Hansen and Manahan-Vaughan, 2014), our results suggest that combining rehabilitation with dopamine agonists could enhance both the saliency of the training signal and the long-term effects on brain plasticity to boost rehabilitation regimens for brain injury.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/jneurosci.4452-15.2016</identifier><identifier>PMID: 27605607</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Adult ; Analysis of Variance ; Domperidone - pharmacology ; Dopamine - metabolism ; Dopamine Agonists - pharmacology ; Dopamine Antagonists - pharmacology ; Ergolines - pharmacology ; Female ; Humans ; Male ; Motion ; Motion Perception - drug effects ; Motion Perception - physiology ; Noise ; Photic Stimulation ; Prolactin - metabolism ; Signal-To-Noise Ratio ; Transcranial Magnetic Stimulation ; Visual Cortex - drug effects ; Visual Cortex - physiology ; Young Adult</subject><ispartof>The Journal of neuroscience, 2016-09, Vol.36 (36), p.9303-9312</ispartof><rights>Copyright © 2016 Yousif et al.</rights><rights>Copyright © 2016 Yousif et al. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c513t-2dd345c669c302309f6ac98a47488dd8d2536ccd4e7c011496fcff69588a3a553</citedby><cites>FETCH-LOGICAL-c513t-2dd345c669c302309f6ac98a47488dd8d2536ccd4e7c011496fcff69588a3a553</cites><orcidid>0000-0002-6578-0904 ; 0000-0001-5473-6038 ; 0000-0003-1402-1091 ; 0000-0002-6794-5813</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/PMC5013183/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5013183/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27605607$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yousif, Nada</creatorcontrib><creatorcontrib>Fu, Richard Z</creatorcontrib><creatorcontrib>Abou-El-Ela Bourquin, Bilal</creatorcontrib><creatorcontrib>Bhrugubanda, Vamsee</creatorcontrib><creatorcontrib>Schultz, Simon R</creatorcontrib><creatorcontrib>Seemungal, Barry M</creatorcontrib><title>Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>When processing sensory signals, the brain must account for noise, both noise in the stimulus and that arising from within its own neuronal circuitry. Dopamine receptor activation is known to enhance both visual cortical signal-to-noise-ratio (SNR) and visual perceptual performance; however, it is unknown whether these two dopamine-mediated phenomena are linked. To assess this, we used single-pulse transcranial magnetic stimulation (TMS) applied to visual cortical area V5/MT to reduce the SNR focally and thus disrupt visual motion discrimination performance to visual targets located in the same retinotopic space. The hypothesis that dopamine receptor activation enhances perceptual performance by improving cortical SNR predicts that dopamine activation should antagonize TMS disruption of visual perception. We assessed this hypothesis via a double-blinded, placebo-controlled study with the dopamine receptor agonists cabergoline (a D2 agonist) and pergolide (a D1/D2 agonist) administered in separate sessions (separated by 2 weeks) in 12 healthy volunteers in a William's balance-order design. TMS degraded visual motion perception when the evoked phosphene and the visual stimulus overlapped in time and space in the placebo and cabergoline conditions, but not in the pergolide condition. This suggests that dopamine D1 or combined D1 and D2 receptor activation enhances cortical SNR to boost perceptual performance. That local visual cortical excitability was unchanged across drug conditions suggests the involvement of long-range intracortical interactions in this D1 effect. Because increased internal noise (and thus lower SNR) can impair visual perceptual learning, improving visual cortical SNR via D1/D2 agonist therapy may be useful in boosting rehabilitation programs involving visual perceptual training.
In this study, we address the issue of whether dopamine activation improves visual perception despite increasing sensory noise in the visual cortex. We show specifically that dopamine D1 (or combined D1/D2) receptor activation enhances the cortical signal-to-noise-ratio to boost perceptual performance. Together with the previously reported effects of dopamine upon brain plasticity and learning (Wolf et al., 2003; Hansen and Manahan-Vaughan, 2014), our results suggest that combining rehabilitation with dopamine agonists could enhance both the saliency of the training signal and the long-term effects on brain plasticity to boost rehabilitation regimens for brain injury.</description><subject>Adult</subject><subject>Analysis of Variance</subject><subject>Domperidone - pharmacology</subject><subject>Dopamine - metabolism</subject><subject>Dopamine Agonists - pharmacology</subject><subject>Dopamine Antagonists - pharmacology</subject><subject>Ergolines - pharmacology</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Motion</subject><subject>Motion Perception - drug effects</subject><subject>Motion Perception - physiology</subject><subject>Noise</subject><subject>Photic Stimulation</subject><subject>Prolactin - metabolism</subject><subject>Signal-To-Noise Ratio</subject><subject>Transcranial Magnetic Stimulation</subject><subject>Visual Cortex - drug effects</subject><subject>Visual Cortex - physiology</subject><subject>Young Adult</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtP3DAQx62qqGwpXwH52EsWv-NckNDy2opHVR5XY5wJGCV2sJOV-u2b7VIEt55mNPOfv2bmh9AeJXMqGd9_DjCmmJ2fCyFZQeWcEao-odnUrQomCP2MZoSVpFCiFNvoa87PhJCS0PIL2malIlKRcobuj2JvOx8AH7rBr-zgY8A_E2RIK8j4zufRtvgibuqQHPR_0yPIvR8AX0afAS_DAKmBBMEBjg0-Gzsb8J3cv7j5hrYa22bYfY076Pbk-GZxVpxfnS4Xh-eFk5QPBatrLqRTqnKcME6qRllXaTstr3Vd65pJrpyrBZSOUCoq1bimUZXU2nIrJd9BBxvffnzooHYQhmRb0yff2fTbROvNx07wT-YxrowklFPNJ4PvrwYpvoyQB9P57KBtbYA4ZkM1KytWMa3-QzoZiunZa6naSN1EKydo3jaixKxJmh-Xx7e_rq4XS7MmOdXMmuQ0uPf-nrexf-j4HywmnKA</recordid><startdate>20160907</startdate><enddate>20160907</enddate><creator>Yousif, Nada</creator><creator>Fu, Richard Z</creator><creator>Abou-El-Ela Bourquin, Bilal</creator><creator>Bhrugubanda, Vamsee</creator><creator>Schultz, Simon R</creator><creator>Seemungal, Barry M</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>7X8</scope><scope>7TK</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6578-0904</orcidid><orcidid>https://orcid.org/0000-0001-5473-6038</orcidid><orcidid>https://orcid.org/0000-0003-1402-1091</orcidid><orcidid>https://orcid.org/0000-0002-6794-5813</orcidid></search><sort><creationdate>20160907</creationdate><title>Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT</title><author>Yousif, Nada ; Fu, Richard Z ; Abou-El-Ela Bourquin, Bilal ; Bhrugubanda, Vamsee ; Schultz, Simon R ; Seemungal, Barry M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-2dd345c669c302309f6ac98a47488dd8d2536ccd4e7c011496fcff69588a3a553</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adult</topic><topic>Analysis of Variance</topic><topic>Domperidone - pharmacology</topic><topic>Dopamine - metabolism</topic><topic>Dopamine Agonists - pharmacology</topic><topic>Dopamine Antagonists - pharmacology</topic><topic>Ergolines - pharmacology</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Motion</topic><topic>Motion Perception - drug effects</topic><topic>Motion Perception - physiology</topic><topic>Noise</topic><topic>Photic Stimulation</topic><topic>Prolactin - metabolism</topic><topic>Signal-To-Noise Ratio</topic><topic>Transcranial Magnetic Stimulation</topic><topic>Visual Cortex - drug effects</topic><topic>Visual Cortex - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yousif, Nada</creatorcontrib><creatorcontrib>Fu, Richard Z</creatorcontrib><creatorcontrib>Abou-El-Ela Bourquin, Bilal</creatorcontrib><creatorcontrib>Bhrugubanda, Vamsee</creatorcontrib><creatorcontrib>Schultz, Simon R</creatorcontrib><creatorcontrib>Seemungal, Barry M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</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>Yousif, Nada</au><au>Fu, Richard Z</au><au>Abou-El-Ela Bourquin, Bilal</au><au>Bhrugubanda, Vamsee</au><au>Schultz, Simon R</au><au>Seemungal, Barry M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2016-09-07</date><risdate>2016</risdate><volume>36</volume><issue>36</issue><spage>9303</spage><epage>9312</epage><pages>9303-9312</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>When processing sensory signals, the brain must account for noise, both noise in the stimulus and that arising from within its own neuronal circuitry. Dopamine receptor activation is known to enhance both visual cortical signal-to-noise-ratio (SNR) and visual perceptual performance; however, it is unknown whether these two dopamine-mediated phenomena are linked. To assess this, we used single-pulse transcranial magnetic stimulation (TMS) applied to visual cortical area V5/MT to reduce the SNR focally and thus disrupt visual motion discrimination performance to visual targets located in the same retinotopic space. The hypothesis that dopamine receptor activation enhances perceptual performance by improving cortical SNR predicts that dopamine activation should antagonize TMS disruption of visual perception. We assessed this hypothesis via a double-blinded, placebo-controlled study with the dopamine receptor agonists cabergoline (a D2 agonist) and pergolide (a D1/D2 agonist) administered in separate sessions (separated by 2 weeks) in 12 healthy volunteers in a William's balance-order design. TMS degraded visual motion perception when the evoked phosphene and the visual stimulus overlapped in time and space in the placebo and cabergoline conditions, but not in the pergolide condition. This suggests that dopamine D1 or combined D1 and D2 receptor activation enhances cortical SNR to boost perceptual performance. That local visual cortical excitability was unchanged across drug conditions suggests the involvement of long-range intracortical interactions in this D1 effect. Because increased internal noise (and thus lower SNR) can impair visual perceptual learning, improving visual cortical SNR via D1/D2 agonist therapy may be useful in boosting rehabilitation programs involving visual perceptual training.
In this study, we address the issue of whether dopamine activation improves visual perception despite increasing sensory noise in the visual cortex. We show specifically that dopamine D1 (or combined D1/D2) receptor activation enhances the cortical signal-to-noise-ratio to boost perceptual performance. Together with the previously reported effects of dopamine upon brain plasticity and learning (Wolf et al., 2003; Hansen and Manahan-Vaughan, 2014), our results suggest that combining rehabilitation with dopamine agonists could enhance both the saliency of the training signal and the long-term effects on brain plasticity to boost rehabilitation regimens for brain injury.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>27605607</pmid><doi>10.1523/jneurosci.4452-15.2016</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-6578-0904</orcidid><orcidid>https://orcid.org/0000-0001-5473-6038</orcidid><orcidid>https://orcid.org/0000-0003-1402-1091</orcidid><orcidid>https://orcid.org/0000-0002-6794-5813</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Analysis of Variance Domperidone - pharmacology Dopamine - metabolism Dopamine Agonists - pharmacology Dopamine Antagonists - pharmacology Ergolines - pharmacology Female Humans Male Motion Motion Perception - drug effects Motion Perception - physiology Noise Photic Stimulation Prolactin - metabolism Signal-To-Noise Ratio Transcranial Magnetic Stimulation Visual Cortex - drug effects Visual Cortex - physiology Young Adult |
title | Dopamine Activation Preserves Visual Motion Perception Despite Noise Interference of Human V5/MT |
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