Mechanisms Underlying Decision-Making as Revealed by Deep-Brain Stimulation in Patients with Parkinson’s Disease
To optimally balance opposing demands of speed and accuracy during decision-making, we must flexibly adapt how much evidence we require before making a choice. Such adjustments in decision thresholds have been linked to the subthalamic nucleus (STN), and therapeutic STN deep-brain stimulation (DBS)...
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Veröffentlicht in: | Current biology 2018-04, Vol.28 (8), p.1169-1178.e6 |
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creator | Herz, Damian M. Little, Simon Pedrosa, David J. Tinkhauser, Gerd Cheeran, Binith Foltynie, Tom Bogacz, Rafal Brown, Peter |
description | To optimally balance opposing demands of speed and accuracy during decision-making, we must flexibly adapt how much evidence we require before making a choice. Such adjustments in decision thresholds have been linked to the subthalamic nucleus (STN), and therapeutic STN deep-brain stimulation (DBS) has been shown to interfere with this function. Here, we performed continuous as well as closed-loop DBS of the STN while Parkinson’s disease patients performed a perceptual decision-making task. Closed-loop STN DBS allowed temporally patterned STN stimulation and simultaneous recordings of STN activity. This revealed that DBS only affected patients’ ability to adjust decision thresholds if applied in a specific temporally confined time window during deliberation. Only stimulation in that window diminished the normal slowing of response times that occurred on difficult trials when DBS was turned off. Furthermore, DBS eliminated a relative, time-specific increase in STN beta oscillations and compromised its functional relationship with trial-by-trial adjustments in decision thresholds. Together, these results provide causal evidence that the STN is involved in adjusting decision thresholds in distinct, time-limited processing windows during deliberation.
•We performed temporally patterned stimulation of the subthalamic nucleus in humans•During stimulation, Parkinson’s patients performed a perceptual decision-making task•Stimulation effects on behavior were confined to a short window during deliberation•Here, stimulation affected changes in decision thresholds during difficult decisions
In this article, Herz et al. provide causal evidence that the subthalamic nucleus mediates adjustments of decision thresholds, depending on the difficulty of the decision. This adjustment is processed during a short time window early during deliberation and is related to changes in oscillatory activity of the subthalamic nucleus. |
doi_str_mv | 10.1016/j.cub.2018.02.057 |
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•We performed temporally patterned stimulation of the subthalamic nucleus in humans•During stimulation, Parkinson’s patients performed a perceptual decision-making task•Stimulation effects on behavior were confined to a short window during deliberation•Here, stimulation affected changes in decision thresholds during difficult decisions
In this article, Herz et al. provide causal evidence that the subthalamic nucleus mediates adjustments of decision thresholds, depending on the difficulty of the decision. This adjustment is processed during a short time window early during deliberation and is related to changes in oscillatory activity of the subthalamic nucleus.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2018.02.057</identifier><identifier>PMID: 29606416</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Aged ; beta ; Cognition - physiology ; Decision Making - physiology ; decision threshold ; decision-making ; Deep Brain Stimulation - methods ; deep-brain stimulation ; drift diffusion model ; Female ; Humans ; Male ; Middle Aged ; Parkinson Disease - physiopathology ; Parkinson’s disease ; Reaction Time ; subthalamic nucleus ; Subthalamic Nucleus - physiology</subject><ispartof>Current biology, 2018-04, Vol.28 (8), p.1169-1178.e6</ispartof><rights>2018 The Authors</rights><rights>Copyright © 2018 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><rights>2018 The Authors 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-4bbc26b3d4b2753c5abfaca9a91383ce6851261e06362e9d3fd7216048347f6e3</citedby><cites>FETCH-LOGICAL-c451t-4bbc26b3d4b2753c5abfaca9a91383ce6851261e06362e9d3fd7216048347f6e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982218302422$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29606416$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Herz, Damian M.</creatorcontrib><creatorcontrib>Little, Simon</creatorcontrib><creatorcontrib>Pedrosa, David J.</creatorcontrib><creatorcontrib>Tinkhauser, Gerd</creatorcontrib><creatorcontrib>Cheeran, Binith</creatorcontrib><creatorcontrib>Foltynie, Tom</creatorcontrib><creatorcontrib>Bogacz, Rafal</creatorcontrib><creatorcontrib>Brown, Peter</creatorcontrib><title>Mechanisms Underlying Decision-Making as Revealed by Deep-Brain Stimulation in Patients with Parkinson’s Disease</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>To optimally balance opposing demands of speed and accuracy during decision-making, we must flexibly adapt how much evidence we require before making a choice. Such adjustments in decision thresholds have been linked to the subthalamic nucleus (STN), and therapeutic STN deep-brain stimulation (DBS) has been shown to interfere with this function. Here, we performed continuous as well as closed-loop DBS of the STN while Parkinson’s disease patients performed a perceptual decision-making task. Closed-loop STN DBS allowed temporally patterned STN stimulation and simultaneous recordings of STN activity. This revealed that DBS only affected patients’ ability to adjust decision thresholds if applied in a specific temporally confined time window during deliberation. Only stimulation in that window diminished the normal slowing of response times that occurred on difficult trials when DBS was turned off. Furthermore, DBS eliminated a relative, time-specific increase in STN beta oscillations and compromised its functional relationship with trial-by-trial adjustments in decision thresholds. Together, these results provide causal evidence that the STN is involved in adjusting decision thresholds in distinct, time-limited processing windows during deliberation.
•We performed temporally patterned stimulation of the subthalamic nucleus in humans•During stimulation, Parkinson’s patients performed a perceptual decision-making task•Stimulation effects on behavior were confined to a short window during deliberation•Here, stimulation affected changes in decision thresholds during difficult decisions
In this article, Herz et al. provide causal evidence that the subthalamic nucleus mediates adjustments of decision thresholds, depending on the difficulty of the decision. This adjustment is processed during a short time window early during deliberation and is related to changes in oscillatory activity of the subthalamic nucleus.</description><subject>Aged</subject><subject>beta</subject><subject>Cognition - physiology</subject><subject>Decision Making - physiology</subject><subject>decision threshold</subject><subject>decision-making</subject><subject>Deep Brain Stimulation - methods</subject><subject>deep-brain stimulation</subject><subject>drift diffusion model</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Parkinson Disease - physiopathology</subject><subject>Parkinson’s disease</subject><subject>Reaction Time</subject><subject>subthalamic nucleus</subject><subject>Subthalamic Nucleus - physiology</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9Uc1u1DAQthCILoUH4IJy5JIwthMnFhIStPxJrUBAz5bjTLpeEmfxJIv2xmvwejwJXm2p4MLJ_vT9zGg-xh5zKDhw9WxTuKUtBPCmAFFAVd9hK97UOoeyrO6yFWgFuW6EOGEPiDYAXDRa3WcnIhGq5GrF4iW6tQ2eRsquQodx2PtwnZ2j8-SnkF_arwdsKfuEO7QDdlm7TzRu81fR-pB9nv24DHZO4izBj-mHYabsu5_XCcVkpyn8-vGTsnNPaAkfsnu9HQgf3byn7OrN6y9n7_KLD2_fn728yF1Z8Tkv29YJ1cqubEVdSVfZtrfOaqu5bKRD1VRcKI6gpBKoO9l3teAKykaWda9QnrIXx9zt0o7YubRWtIPZRj_auDeT9eZfJvi1uZ52ptJcaBAp4OlNQJy-LUizGT05HAYbcFrICBDQ6LqWMkn5UeriRBSxvx3DwRy6MhuTujKHrgwIk7pKnid_73fr-FNOEjw_CjBdaecxGnLpuA47H9HNppv8f-J_A5HGp9g</recordid><startdate>20180423</startdate><enddate>20180423</enddate><creator>Herz, Damian M.</creator><creator>Little, Simon</creator><creator>Pedrosa, David J.</creator><creator>Tinkhauser, Gerd</creator><creator>Cheeran, Binith</creator><creator>Foltynie, Tom</creator><creator>Bogacz, Rafal</creator><creator>Brown, Peter</creator><general>Elsevier Ltd</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><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>5PM</scope></search><sort><creationdate>20180423</creationdate><title>Mechanisms Underlying Decision-Making as Revealed by Deep-Brain Stimulation in Patients with Parkinson’s Disease</title><author>Herz, Damian M. ; Little, Simon ; Pedrosa, David J. ; Tinkhauser, Gerd ; Cheeran, Binith ; Foltynie, Tom ; Bogacz, Rafal ; Brown, Peter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-4bbc26b3d4b2753c5abfaca9a91383ce6851261e06362e9d3fd7216048347f6e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Aged</topic><topic>beta</topic><topic>Cognition - physiology</topic><topic>Decision Making - physiology</topic><topic>decision threshold</topic><topic>decision-making</topic><topic>Deep Brain Stimulation - methods</topic><topic>deep-brain stimulation</topic><topic>drift diffusion model</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Parkinson Disease - physiopathology</topic><topic>Parkinson’s disease</topic><topic>Reaction Time</topic><topic>subthalamic nucleus</topic><topic>Subthalamic Nucleus - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Herz, Damian M.</creatorcontrib><creatorcontrib>Little, Simon</creatorcontrib><creatorcontrib>Pedrosa, David J.</creatorcontrib><creatorcontrib>Tinkhauser, Gerd</creatorcontrib><creatorcontrib>Cheeran, Binith</creatorcontrib><creatorcontrib>Foltynie, Tom</creatorcontrib><creatorcontrib>Bogacz, Rafal</creatorcontrib><creatorcontrib>Brown, Peter</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Herz, Damian M.</au><au>Little, Simon</au><au>Pedrosa, David J.</au><au>Tinkhauser, Gerd</au><au>Cheeran, Binith</au><au>Foltynie, Tom</au><au>Bogacz, Rafal</au><au>Brown, Peter</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mechanisms Underlying Decision-Making as Revealed by Deep-Brain Stimulation in Patients with Parkinson’s Disease</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2018-04-23</date><risdate>2018</risdate><volume>28</volume><issue>8</issue><spage>1169</spage><epage>1178.e6</epage><pages>1169-1178.e6</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>To optimally balance opposing demands of speed and accuracy during decision-making, we must flexibly adapt how much evidence we require before making a choice. Such adjustments in decision thresholds have been linked to the subthalamic nucleus (STN), and therapeutic STN deep-brain stimulation (DBS) has been shown to interfere with this function. Here, we performed continuous as well as closed-loop DBS of the STN while Parkinson’s disease patients performed a perceptual decision-making task. Closed-loop STN DBS allowed temporally patterned STN stimulation and simultaneous recordings of STN activity. This revealed that DBS only affected patients’ ability to adjust decision thresholds if applied in a specific temporally confined time window during deliberation. Only stimulation in that window diminished the normal slowing of response times that occurred on difficult trials when DBS was turned off. Furthermore, DBS eliminated a relative, time-specific increase in STN beta oscillations and compromised its functional relationship with trial-by-trial adjustments in decision thresholds. Together, these results provide causal evidence that the STN is involved in adjusting decision thresholds in distinct, time-limited processing windows during deliberation.
•We performed temporally patterned stimulation of the subthalamic nucleus in humans•During stimulation, Parkinson’s patients performed a perceptual decision-making task•Stimulation effects on behavior were confined to a short window during deliberation•Here, stimulation affected changes in decision thresholds during difficult decisions
In this article, Herz et al. provide causal evidence that the subthalamic nucleus mediates adjustments of decision thresholds, depending on the difficulty of the decision. This adjustment is processed during a short time window early during deliberation and is related to changes in oscillatory activity of the subthalamic nucleus.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>29606416</pmid><doi>10.1016/j.cub.2018.02.057</doi><oa>free_for_read</oa></addata></record> |
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subjects | Aged beta Cognition - physiology Decision Making - physiology decision threshold decision-making Deep Brain Stimulation - methods deep-brain stimulation drift diffusion model Female Humans Male Middle Aged Parkinson Disease - physiopathology Parkinson’s disease Reaction Time subthalamic nucleus Subthalamic Nucleus - physiology |
title | Mechanisms Underlying Decision-Making as Revealed by Deep-Brain Stimulation in Patients with Parkinson’s Disease |
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