Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.
Identifieur interne : 000457 ( PubMed/Corpus ); précédent : 000456; suivant : 000458Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.
Auteurs : Liping Wang ; Xianchun Li ; Steven S. Hsiao ; Fred A. Lenz ; Mark Bodner ; Yong-Di Zhou ; Joaquín M. FusterSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2015.
English descriptors
- KwdEn :
- Animals, Eye Movements (physiology), Female, Macaca mulatta (physiology), Macaca mulatta (psychology), Male, Memory, Short-Term (physiology), Neurons (physiology), Photic Stimulation, Physical Stimulation, Prefrontal Cortex (physiology), Task Performance and Analysis, Time Factors, Touch Perception (physiology), Visual Perception (physiology).
- MESH :
- physiology : Eye Movements, Macaca mulatta, Memory, Short-Term, Neurons, Prefrontal Cortex, Touch Perception, Visual Perception.
- psychology : Macaca mulatta.
- Animals, Female, Male, Photic Stimulation, Physical Stimulation, Task Performance and Analysis, Time Factors.
Abstract
Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal activity recorded in the DLPFC in the delay period of both tasks indicates that the early-delay differential activity probably is related to the encoding of sample information with different strengths depending on task modality, that the late-delay differential activity reflects the associated (modality-independent) action component of haptic choice in both tasks (that is, the anticipation of the behavioral choice and/or active recall and maintenance of sample information for subsequent action), and that the sustained whole-delay differential activity likely bridges and integrates the sensory and action components. In addition, the VH late-delay differential activity was significantly diminished when the haptic choice was not required. Taken together, the results show that, in addition to the whole-delay differential activity, DLPFC neurons also show early- and late-delay differential activities. These previously unidentified findings indicate that DLPFC is capable of (i) holding the coded sample information (e.g., visual or tactile information) in the early-delay activity, (ii) retrieving the abstract information (orientations) of the sample (whether the sample has been haptic or visual) and holding it in the late-delay activity, and (iii) preparing for behavioral choice acting on that abstract information.
DOI: 10.1073/pnas.1410130112
PubMed: 25540412
Links to Exploration step
pubmed:25540412Le document en format XML
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Hsiao</name><affiliation><nlm:affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21205;</nlm:affiliation></affiliation></author><author><name sortKey="Lenz, Fred A" sort="Lenz, Fred A" uniqKey="Lenz F" first="Fred A" last="Lenz">Fred A. Lenz</name><affiliation><nlm:affiliation>Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287;</nlm:affiliation></affiliation></author><author><name sortKey="Bodner, Mark" sort="Bodner, Mark" uniqKey="Bodner M" first="Mark" last="Bodner">Mark Bodner</name><affiliation><nlm:affiliation>MIND Research Institute, Irvine, CA 92617; and.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Yong Di" sort="Zhou, Yong Di" uniqKey="Zhou Y" first="Yong-Di" last="Zhou">Yong-Di Zhou</name><affiliation><nlm:affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287; yzhou12@jhmi.edu.</nlm:affiliation></affiliation></author><author><name sortKey="Fuster, Joaquin M" sort="Fuster, Joaquin M" uniqKey="Fuster J" first="Joaquín M" last="Fuster">Joaquín M. Fuster</name><affiliation><nlm:affiliation>Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90024.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2015">2015</date><idno type="RBID">pubmed:25540412</idno><idno type="pmid">25540412</idno><idno type="doi">10.1073/pnas.1410130112</idno><idno type="wicri:Area/PubMed/Corpus">000457</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.</title><author><name sortKey="Wang, Liping" sort="Wang, Liping" uniqKey="Wang L" first="Liping" last="Wang">Liping Wang</name><affiliation><nlm:affiliation>Key Laboratory of Brain Functional Genomics (Ministry of Education & Science and Technology Commission of Shanghai Municipality), Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China; NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China;</nlm:affiliation></affiliation></author><author><name sortKey="Li, Xianchun" sort="Li, Xianchun" uniqKey="Li X" first="Xianchun" last="Li">Xianchun Li</name><affiliation><nlm:affiliation>Key Laboratory of Brain Functional Genomics (Ministry of Education & Science and Technology Commission of Shanghai Municipality), Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China;</nlm:affiliation></affiliation></author><author><name sortKey="Hsiao, Steven S" sort="Hsiao, Steven S" uniqKey="Hsiao S" first="Steven S" last="Hsiao">Steven S. Hsiao</name><affiliation><nlm:affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21205;</nlm:affiliation></affiliation></author><author><name sortKey="Lenz, Fred A" sort="Lenz, Fred A" uniqKey="Lenz F" first="Fred A" last="Lenz">Fred A. Lenz</name><affiliation><nlm:affiliation>Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287;</nlm:affiliation></affiliation></author><author><name sortKey="Bodner, Mark" sort="Bodner, Mark" uniqKey="Bodner M" first="Mark" last="Bodner">Mark Bodner</name><affiliation><nlm:affiliation>MIND Research Institute, Irvine, CA 92617; and.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Yong Di" sort="Zhou, Yong Di" uniqKey="Zhou Y" first="Yong-Di" last="Zhou">Yong-Di Zhou</name><affiliation><nlm:affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287; yzhou12@jhmi.edu.</nlm:affiliation></affiliation></author><author><name sortKey="Fuster, Joaquin M" sort="Fuster, Joaquin M" uniqKey="Fuster J" first="Joaquín M" last="Fuster">Joaquín M. Fuster</name><affiliation><nlm:affiliation>Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90024.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Eye Movements (physiology)</term><term>Female</term><term>Macaca mulatta (physiology)</term><term>Macaca mulatta (psychology)</term><term>Male</term><term>Memory, Short-Term (physiology)</term><term>Neurons (physiology)</term><term>Photic Stimulation</term><term>Physical Stimulation</term><term>Prefrontal Cortex (physiology)</term><term>Task Performance and Analysis</term><term>Time Factors</term><term>Touch Perception (physiology)</term><term>Visual Perception (physiology)</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Eye Movements</term><term>Macaca mulatta</term><term>Memory, Short-Term</term><term>Neurons</term><term>Prefrontal Cortex</term><term>Touch Perception</term><term>Visual Perception</term></keywords><keywords scheme="MESH" qualifier="psychology" xml:lang="en"><term>Macaca mulatta</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Female</term><term>Male</term><term>Photic Stimulation</term><term>Physical Stimulation</term><term>Task Performance and Analysis</term><term>Time Factors</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal activity recorded in the DLPFC in the delay period of both tasks indicates that the early-delay differential activity probably is related to the encoding of sample information with different strengths depending on task modality, that the late-delay differential activity reflects the associated (modality-independent) action component of haptic choice in both tasks (that is, the anticipation of the behavioral choice and/or active recall and maintenance of sample information for subsequent action), and that the sustained whole-delay differential activity likely bridges and integrates the sensory and action components. In addition, the VH late-delay differential activity was significantly diminished when the haptic choice was not required. Taken together, the results show that, in addition to the whole-delay differential activity, DLPFC neurons also show early- and late-delay differential activities. These previously unidentified findings indicate that DLPFC is capable of (i) holding the coded sample information (e.g., visual or tactile information) in the early-delay activity, (ii) retrieving the abstract information (orientations) of the sample (whether the sample has been haptic or visual) and holding it in the late-delay activity, and (iii) preparing for behavioral choice acting on that abstract information.</div></front></TEI><pubmed><MedlineCitation Owner="NLM" Status="MEDLINE"><PMID Version="1">25540412</PMID><DateCreated><Year>2015</Year><Month>01</Month><Day>14</Day></DateCreated><DateCompleted><Year>2015</Year><Month>04</Month><Day>30</Day></DateCompleted><DateRevised><Year>2015</Year><Month>10</Month><Day>28</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>112</Volume><Issue>2</Issue><PubDate><Year>2015</Year><Month>Jan</Month><Day>13</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc. Natl. Acad. Sci. U.S.A.</ISOAbbreviation></Journal><ArticleTitle>Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.</ArticleTitle><Pagination><MedlinePgn>E214-9</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1410130112</ELocationID><Abstract><AbstractText>Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal activity recorded in the DLPFC in the delay period of both tasks indicates that the early-delay differential activity probably is related to the encoding of sample information with different strengths depending on task modality, that the late-delay differential activity reflects the associated (modality-independent) action component of haptic choice in both tasks (that is, the anticipation of the behavioral choice and/or active recall and maintenance of sample information for subsequent action), and that the sustained whole-delay differential activity likely bridges and integrates the sensory and action components. In addition, the VH late-delay differential activity was significantly diminished when the haptic choice was not required. Taken together, the results show that, in addition to the whole-delay differential activity, DLPFC neurons also show early- and late-delay differential activities. These previously unidentified findings indicate that DLPFC is capable of (i) holding the coded sample information (e.g., visual or tactile information) in the early-delay activity, (ii) retrieving the abstract information (orientations) of the sample (whether the sample has been haptic or visual) and holding it in the late-delay activity, and (iii) preparing for behavioral choice acting on that abstract information.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Liping</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Key Laboratory of Brain Functional Genomics (Ministry of Education & Science and Technology Commission of Shanghai Municipality), Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China; NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China;</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Xianchun</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Key Laboratory of Brain Functional Genomics (Ministry of Education & Science and Technology Commission of Shanghai Municipality), Institute of Cognitive Neuroscience, School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China;</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hsiao</LastName><ForeName>Steven S</ForeName><Initials>SS</Initials><AffiliationInfo><Affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21205;</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lenz</LastName><ForeName>Fred A</ForeName><Initials>FA</Initials><AffiliationInfo><Affiliation>Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287;</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bodner</LastName><ForeName>Mark</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>MIND Research Institute, Irvine, CA 92617; and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Yong-Di</ForeName><Initials>YD</Initials><AffiliationInfo><Affiliation>Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218; Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287; yzhou12@jhmi.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fuster</LastName><ForeName>Joaquín M</ForeName><Initials>JM</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-0681-6444</Identifier><AffiliationInfo><Affiliation>Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90024.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>NS-44919</GrantID><Acronym>NS</Acronym><Agency>NINDS NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 NS038493</GrantID><Acronym>NS</Acronym><Agency>NINDS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>12</Month><Day>24</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Nature. 2000 May 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