Low-dimensional dynamics for working memory and time encoding
Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during...
Gespeichert in:
Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2020-09, Vol.117 (37), p.23021-23032 |
---|---|
Hauptverfasser: | , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 23032 |
---|---|
container_issue | 37 |
container_start_page | 23021 |
container_title | Proceedings of the National Academy of Sciences - PNAS |
container_volume | 117 |
creator | Cueva, Christopher J. Saez, Alex Marcos, Encarni Genovesio, Aldo Jazayeri, Mehrdad Romo, Ranulfo Salzman, C. Daniel Shadlen, Michael N. Fusi, Stefano |
description | Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear “ramping” component of each neuron’s firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data. |
doi_str_mv | 10.1073/pnas.1915984117 |
format | Article |
fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7502752</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26969233</jstor_id><sourcerecordid>26969233</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-ad4c355d80193557b65e79e8f263d432e82daa50643b1a0ec4f2547f3af9d4ac3</originalsourceid><addsrcrecordid>eNpdkUtLAzEUhYMoWh9rV8qAGzejeU6ShYKILyi40XVIk0ydOpPUZGrpvzeltT5Wd3G-e7j3HACOEbxAkJPLqdfpAknEpKAI8S0wQFCisqISboMBhJiXgmK6B_ZTmkAIJRNwF-wRLJjkrBqAq2GYl7bpnE9N8Lot7MLrrjGpqEMs5iG-N35cdK4LcVFob4s-s4XzJtgsHIKdWrfJHa3nAXi9v3u5fSyHzw9PtzfD0lBK-lJbaghjVkAk8-SjijkunahxRSwl2AlstWawomSENHSG1phRXhNdS0u1IQfgeuU7nY06Z43zfdStmsam03Ghgm7UX8U3b2ocPhVnOQKGs8H52iCGj5lLveqaZFzbau_CLClMiai4IBxl9OwfOgmzmKNZUpQTyDKaqcsVZWJIKbp6cwyCalmNWlajfqrJG6e_f9jw311k4GQFTFIf4kbHlawkJoR8AX6ilEo</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2447305386</pqid></control><display><type>article</type><title>Low-dimensional dynamics for working memory and time encoding</title><source>MEDLINE</source><source>JSTOR Archive Collection A-Z Listing</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Cueva, Christopher J. ; Saez, Alex ; Marcos, Encarni ; Genovesio, Aldo ; Jazayeri, Mehrdad ; Romo, Ranulfo ; Salzman, C. Daniel ; Shadlen, Michael N. ; Fusi, Stefano</creator><creatorcontrib>Cueva, Christopher J. ; Saez, Alex ; Marcos, Encarni ; Genovesio, Aldo ; Jazayeri, Mehrdad ; Romo, Ranulfo ; Salzman, C. Daniel ; Shadlen, Michael N. ; Fusi, Stefano</creatorcontrib><description>Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear “ramping” component of each neuron’s firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1915984117</identifier><identifier>PMID: 32859756</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Back propagation ; Back propagation networks ; Biological Sciences ; Brain - physiology ; Brain Mapping - methods ; Constraint modelling ; Firing rate ; Memory, Short-Term - physiology ; Nerve Net - physiology ; Neural networks ; Neural Networks, Computer ; Neurons - physiology ; Primates ; Short term memory ; Timing</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2020-09, Vol.117 (37), p.23021-23032</ispartof><rights>Copyright National Academy of Sciences Sep 15, 2020</rights><rights>2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-ad4c355d80193557b65e79e8f263d432e82daa50643b1a0ec4f2547f3af9d4ac3</citedby><cites>FETCH-LOGICAL-c443t-ad4c355d80193557b65e79e8f263d432e82daa50643b1a0ec4f2547f3af9d4ac3</cites><orcidid>0000-0002-3035-6652 ; 0000-0002-9764-6961</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26969233$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26969233$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32859756$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cueva, Christopher J.</creatorcontrib><creatorcontrib>Saez, Alex</creatorcontrib><creatorcontrib>Marcos, Encarni</creatorcontrib><creatorcontrib>Genovesio, Aldo</creatorcontrib><creatorcontrib>Jazayeri, Mehrdad</creatorcontrib><creatorcontrib>Romo, Ranulfo</creatorcontrib><creatorcontrib>Salzman, C. Daniel</creatorcontrib><creatorcontrib>Shadlen, Michael N.</creatorcontrib><creatorcontrib>Fusi, Stefano</creatorcontrib><title>Low-dimensional dynamics for working memory and time encoding</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear “ramping” component of each neuron’s firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data.</description><subject>Animals</subject><subject>Back propagation</subject><subject>Back propagation networks</subject><subject>Biological Sciences</subject><subject>Brain - physiology</subject><subject>Brain Mapping - methods</subject><subject>Constraint modelling</subject><subject>Firing rate</subject><subject>Memory, Short-Term - physiology</subject><subject>Nerve Net - physiology</subject><subject>Neural networks</subject><subject>Neural Networks, Computer</subject><subject>Neurons - physiology</subject><subject>Primates</subject><subject>Short term memory</subject><subject>Timing</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtLAzEUhYMoWh9rV8qAGzejeU6ShYKILyi40XVIk0ydOpPUZGrpvzeltT5Wd3G-e7j3HACOEbxAkJPLqdfpAknEpKAI8S0wQFCisqISboMBhJiXgmK6B_ZTmkAIJRNwF-wRLJjkrBqAq2GYl7bpnE9N8Lot7MLrrjGpqEMs5iG-N35cdK4LcVFob4s-s4XzJtgsHIKdWrfJHa3nAXi9v3u5fSyHzw9PtzfD0lBK-lJbaghjVkAk8-SjijkunahxRSwl2AlstWawomSENHSG1phRXhNdS0u1IQfgeuU7nY06Z43zfdStmsam03Ghgm7UX8U3b2ocPhVnOQKGs8H52iCGj5lLveqaZFzbau_CLClMiai4IBxl9OwfOgmzmKNZUpQTyDKaqcsVZWJIKbp6cwyCalmNWlajfqrJG6e_f9jw311k4GQFTFIf4kbHlawkJoR8AX6ilEo</recordid><startdate>20200915</startdate><enddate>20200915</enddate><creator>Cueva, Christopher J.</creator><creator>Saez, Alex</creator><creator>Marcos, Encarni</creator><creator>Genovesio, Aldo</creator><creator>Jazayeri, Mehrdad</creator><creator>Romo, Ranulfo</creator><creator>Salzman, C. Daniel</creator><creator>Shadlen, Michael N.</creator><creator>Fusi, Stefano</creator><general>National Academy of Sciences</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3035-6652</orcidid><orcidid>https://orcid.org/0000-0002-9764-6961</orcidid></search><sort><creationdate>20200915</creationdate><title>Low-dimensional dynamics for working memory and time encoding</title><author>Cueva, Christopher J. ; Saez, Alex ; Marcos, Encarni ; Genovesio, Aldo ; Jazayeri, Mehrdad ; Romo, Ranulfo ; Salzman, C. Daniel ; Shadlen, Michael N. ; Fusi, Stefano</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-ad4c355d80193557b65e79e8f263d432e82daa50643b1a0ec4f2547f3af9d4ac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Back propagation</topic><topic>Back propagation networks</topic><topic>Biological Sciences</topic><topic>Brain - physiology</topic><topic>Brain Mapping - methods</topic><topic>Constraint modelling</topic><topic>Firing rate</topic><topic>Memory, Short-Term - physiology</topic><topic>Nerve Net - physiology</topic><topic>Neural networks</topic><topic>Neural Networks, Computer</topic><topic>Neurons - physiology</topic><topic>Primates</topic><topic>Short term memory</topic><topic>Timing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cueva, Christopher J.</creatorcontrib><creatorcontrib>Saez, Alex</creatorcontrib><creatorcontrib>Marcos, Encarni</creatorcontrib><creatorcontrib>Genovesio, Aldo</creatorcontrib><creatorcontrib>Jazayeri, Mehrdad</creatorcontrib><creatorcontrib>Romo, Ranulfo</creatorcontrib><creatorcontrib>Salzman, C. Daniel</creatorcontrib><creatorcontrib>Shadlen, Michael N.</creatorcontrib><creatorcontrib>Fusi, Stefano</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cueva, Christopher J.</au><au>Saez, Alex</au><au>Marcos, Encarni</au><au>Genovesio, Aldo</au><au>Jazayeri, Mehrdad</au><au>Romo, Ranulfo</au><au>Salzman, C. Daniel</au><au>Shadlen, Michael N.</au><au>Fusi, Stefano</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Low-dimensional dynamics for working memory and time encoding</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2020-09-15</date><risdate>2020</risdate><volume>117</volume><issue>37</issue><spage>23021</spage><epage>23032</epage><pages>23021-23032</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear “ramping” component of each neuron’s firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>32859756</pmid><doi>10.1073/pnas.1915984117</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-3035-6652</orcidid><orcidid>https://orcid.org/0000-0002-9764-6961</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0027-8424 |
ispartof | Proceedings of the National Academy of Sciences - PNAS, 2020-09, Vol.117 (37), p.23021-23032 |
issn | 0027-8424 1091-6490 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7502752 |
source | MEDLINE; JSTOR Archive Collection A-Z Listing; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
subjects | Animals Back propagation Back propagation networks Biological Sciences Brain - physiology Brain Mapping - methods Constraint modelling Firing rate Memory, Short-Term - physiology Nerve Net - physiology Neural networks Neural Networks, Computer Neurons - physiology Primates Short term memory Timing |
title | Low-dimensional dynamics for working memory and time encoding |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T07%3A22%3A56IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Low-dimensional%20dynamics%20for%20working%20memory%20and%20time%20encoding&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Cueva,%20Christopher%20J.&rft.date=2020-09-15&rft.volume=117&rft.issue=37&rft.spage=23021&rft.epage=23032&rft.pages=23021-23032&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1915984117&rft_dat=%3Cjstor_pubme%3E26969233%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2447305386&rft_id=info:pmid/32859756&rft_jstor_id=26969233&rfr_iscdi=true |