Olfactory network dynamics and the coding of multidimensional signals

Key Points The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects that we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. The olfactory system therefore solves complicated patt...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Nature reviews. Neuroscience 2002-11, Vol.3 (11), p.884-895
1. Verfasser: Laurent, Gilles
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 895
container_issue 11
container_start_page 884
container_title Nature reviews. Neuroscience
container_volume 3
creator Laurent, Gilles
description Key Points The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects that we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. The olfactory system therefore solves complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimize their distribution within it. This process uses both oscillatory and non-periodic dynamic processes that serve complementary roles: slow non-periodic processes allow decorrelation (that is, the reduction of the overlap between odour representations); fast oscillations allow sparsening (that is, a reduction in the size of the coding assemblies) and feature binding (that is, the representation of multiple and co-occurring features by the spikes of single neurons). The prominent role of oscillatory synchronization in the process of sparsening is reviewed. Briefly, sparsening is achieved through a process that involves periodic input, coincidence detection, fan-in and fan-out connection patterns, and delayed feedforward inhibition. These mechanisms together lead to the appearance of rare but highly selective neuronal responses, which synthesize specific combinations of input features. The coding aspects, advantages, disadvantages and possible uses of these interlocked and dynamic integrative phenomena are discussed in the context of olfaction and other systems in which complex sensory objects must be represented, learned and recognized. The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects, which we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. This means that the olfactory system must solve complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimizes their distribution within it. This process uses both oscillatory and non-periodic dynamic processes wit
doi_str_mv 10.1038/nrn964
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_72643674</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>72643674</sourcerecordid><originalsourceid>FETCH-LOGICAL-c431t-bfa3f5d5bd14af6083c07bc6a1f51fcbc32313c337d76749c9b00f4abe9430b13</originalsourceid><addsrcrecordid>eNqFkE1Lw0AQhhdRrFb9CRI86Cm6k9lskqOU-gGFXhS8hc1-1NRkt-4mSP-9KS0WevH0LsyzzzAvIVdA74Fi_mC9LTg7ImfAMogpZfnx3xs_RuQ8hCWlwCHjp2QECYM0KfgZmc4bI2Tn_Dqyuvtx_itSayvaWoZIWBV1nzqSTtV2ETkTtX3T1aputQ21s6KJQr0YIlyQEzOEvtzlmLw_Td8mL_Fs_vw6eZzFkiF0cWUEmlSllQImDKc5SppVkgswKRhZSUwQUCJmKuMZK2RRUWqYqHTBkFaAY3K79a68--516Mq2DlI3jbDa9aHMEs5w-PkvCDkHZIgDeHMALl3vNzeVSUIBecJwb5PeheC1KVe-boVfl0DLTf3ltv4BvN7Z-qrVao_t-h6Auy0QhpFdaL9fd6D6BZQ5jP4</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>220136243</pqid></control><display><type>article</type><title>Olfactory network dynamics and the coding of multidimensional signals</title><source>MEDLINE</source><source>SpringerLink Journals</source><source>Nature</source><creator>Laurent, Gilles</creator><creatorcontrib>Laurent, Gilles</creatorcontrib><description>Key Points The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects that we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. The olfactory system therefore solves complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimize their distribution within it. This process uses both oscillatory and non-periodic dynamic processes that serve complementary roles: slow non-periodic processes allow decorrelation (that is, the reduction of the overlap between odour representations); fast oscillations allow sparsening (that is, a reduction in the size of the coding assemblies) and feature binding (that is, the representation of multiple and co-occurring features by the spikes of single neurons). The prominent role of oscillatory synchronization in the process of sparsening is reviewed. Briefly, sparsening is achieved through a process that involves periodic input, coincidence detection, fan-in and fan-out connection patterns, and delayed feedforward inhibition. These mechanisms together lead to the appearance of rare but highly selective neuronal responses, which synthesize specific combinations of input features. The coding aspects, advantages, disadvantages and possible uses of these interlocked and dynamic integrative phenomena are discussed in the context of olfaction and other systems in which complex sensory objects must be represented, learned and recognized. The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects, which we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. This means that the olfactory system must solve complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimizes their distribution within it. This process uses both oscillatory and non-periodic dynamic processes with complementary functions: slow non-periodic processes underlie decorrelation, whereas fast oscillations allow sparsening and feature binding.</description><identifier>ISSN: 1471-003X</identifier><identifier>ISSN: 1471-0048</identifier><identifier>EISSN: 1471-0048</identifier><identifier>EISSN: 1469-3178</identifier><identifier>DOI: 10.1038/nrn964</identifier><identifier>PMID: 12415296</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Animal Genetics and Genomics ; Animals ; Behavioral Sciences ; Biological Techniques ; Biomedical and Life Sciences ; Biomedicine ; Brain ; Ganglia, Invertebrate - cytology ; Ganglia, Invertebrate - physiology ; Humans ; Hypotheses ; Muscular Dystrophy, Animal ; Nerve Net - cytology ; Nerve Net - physiology ; Neurobiology ; Neurons ; Neurons - physiology ; Neurosciences ; Olfactory Bulb - cytology ; Olfactory Bulb - physiology ; Olfactory Pathways - cytology ; Olfactory Pathways - physiology ; review-article ; Signal Transduction - physiology ; Smell - physiology ; Synaptic Transmission - physiology</subject><ispartof>Nature reviews. Neuroscience, 2002-11, Vol.3 (11), p.884-895</ispartof><rights>Springer Nature Limited 2002</rights><rights>Copyright Nature Publishing Group Nov 2002</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c431t-bfa3f5d5bd14af6083c07bc6a1f51fcbc32313c337d76749c9b00f4abe9430b13</citedby><cites>FETCH-LOGICAL-c431t-bfa3f5d5bd14af6083c07bc6a1f51fcbc32313c337d76749c9b00f4abe9430b13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nrn964$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nrn964$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27903,27904,41467,42536,51297</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12415296$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Laurent, Gilles</creatorcontrib><title>Olfactory network dynamics and the coding of multidimensional signals</title><title>Nature reviews. Neuroscience</title><addtitle>Nat Rev Neurosci</addtitle><addtitle>Nat Rev Neurosci</addtitle><description>Key Points The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects that we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. The olfactory system therefore solves complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimize their distribution within it. This process uses both oscillatory and non-periodic dynamic processes that serve complementary roles: slow non-periodic processes allow decorrelation (that is, the reduction of the overlap between odour representations); fast oscillations allow sparsening (that is, a reduction in the size of the coding assemblies) and feature binding (that is, the representation of multiple and co-occurring features by the spikes of single neurons). The prominent role of oscillatory synchronization in the process of sparsening is reviewed. Briefly, sparsening is achieved through a process that involves periodic input, coincidence detection, fan-in and fan-out connection patterns, and delayed feedforward inhibition. These mechanisms together lead to the appearance of rare but highly selective neuronal responses, which synthesize specific combinations of input features. The coding aspects, advantages, disadvantages and possible uses of these interlocked and dynamic integrative phenomena are discussed in the context of olfaction and other systems in which complex sensory objects must be represented, learned and recognized. The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects, which we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. This means that the olfactory system must solve complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimizes their distribution within it. This process uses both oscillatory and non-periodic dynamic processes with complementary functions: slow non-periodic processes underlie decorrelation, whereas fast oscillations allow sparsening and feature binding.</description><subject>Animal Genetics and Genomics</subject><subject>Animals</subject><subject>Behavioral Sciences</subject><subject>Biological Techniques</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Ganglia, Invertebrate - cytology</subject><subject>Ganglia, Invertebrate - physiology</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Muscular Dystrophy, Animal</subject><subject>Nerve Net - cytology</subject><subject>Nerve Net - physiology</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Neurosciences</subject><subject>Olfactory Bulb - cytology</subject><subject>Olfactory Bulb - physiology</subject><subject>Olfactory Pathways - cytology</subject><subject>Olfactory Pathways - physiology</subject><subject>review-article</subject><subject>Signal Transduction - physiology</subject><subject>Smell - physiology</subject><subject>Synaptic Transmission - physiology</subject><issn>1471-003X</issn><issn>1471-0048</issn><issn>1471-0048</issn><issn>1469-3178</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2002</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkE1Lw0AQhhdRrFb9CRI86Cm6k9lskqOU-gGFXhS8hc1-1NRkt-4mSP-9KS0WevH0LsyzzzAvIVdA74Fi_mC9LTg7ImfAMogpZfnx3xs_RuQ8hCWlwCHjp2QECYM0KfgZmc4bI2Tn_Dqyuvtx_itSayvaWoZIWBV1nzqSTtV2ETkTtX3T1aputQ21s6KJQr0YIlyQEzOEvtzlmLw_Td8mL_Fs_vw6eZzFkiF0cWUEmlSllQImDKc5SppVkgswKRhZSUwQUCJmKuMZK2RRUWqYqHTBkFaAY3K79a68--516Mq2DlI3jbDa9aHMEs5w-PkvCDkHZIgDeHMALl3vNzeVSUIBecJwb5PeheC1KVe-boVfl0DLTf3ltv4BvN7Z-qrVao_t-h6Auy0QhpFdaL9fd6D6BZQ5jP4</recordid><startdate>20021101</startdate><enddate>20021101</enddate><creator>Laurent, Gilles</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20021101</creationdate><title>Olfactory network dynamics and the coding of multidimensional signals</title><author>Laurent, Gilles</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c431t-bfa3f5d5bd14af6083c07bc6a1f51fcbc32313c337d76749c9b00f4abe9430b13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2002</creationdate><topic>Animal Genetics and Genomics</topic><topic>Animals</topic><topic>Behavioral Sciences</topic><topic>Biological Techniques</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Brain</topic><topic>Ganglia, Invertebrate - cytology</topic><topic>Ganglia, Invertebrate - physiology</topic><topic>Humans</topic><topic>Hypotheses</topic><topic>Muscular Dystrophy, Animal</topic><topic>Nerve Net - cytology</topic><topic>Nerve Net - physiology</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Neurosciences</topic><topic>Olfactory Bulb - cytology</topic><topic>Olfactory Bulb - physiology</topic><topic>Olfactory Pathways - cytology</topic><topic>Olfactory Pathways - physiology</topic><topic>review-article</topic><topic>Signal Transduction - physiology</topic><topic>Smell - physiology</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Laurent, Gilles</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Psychology</collection><collection>Biological Science Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Nature reviews. Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Laurent, Gilles</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Olfactory network dynamics and the coding of multidimensional signals</atitle><jtitle>Nature reviews. Neuroscience</jtitle><stitle>Nat Rev Neurosci</stitle><addtitle>Nat Rev Neurosci</addtitle><date>2002-11-01</date><risdate>2002</risdate><volume>3</volume><issue>11</issue><spage>884</spage><epage>895</epage><pages>884-895</pages><issn>1471-003X</issn><issn>1471-0048</issn><eissn>1471-0048</eissn><eissn>1469-3178</eissn><abstract>Key Points The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects that we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. The olfactory system therefore solves complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimize their distribution within it. This process uses both oscillatory and non-periodic dynamic processes that serve complementary roles: slow non-periodic processes allow decorrelation (that is, the reduction of the overlap between odour representations); fast oscillations allow sparsening (that is, a reduction in the size of the coding assemblies) and feature binding (that is, the representation of multiple and co-occurring features by the spikes of single neurons). The prominent role of oscillatory synchronization in the process of sparsening is reviewed. Briefly, sparsening is achieved through a process that involves periodic input, coincidence detection, fan-in and fan-out connection patterns, and delayed feedforward inhibition. These mechanisms together lead to the appearance of rare but highly selective neuronal responses, which synthesize specific combinations of input features. The coding aspects, advantages, disadvantages and possible uses of these interlocked and dynamic integrative phenomena are discussed in the context of olfaction and other systems in which complex sensory objects must be represented, learned and recognized. The brain faces many complex problems when dealing with odorant signals. Odours are multidimensional objects, which we usually experience as unitary percepts. They are also noisy and variable, but we can classify and identify them well. This means that the olfactory system must solve complicated pattern-learning and pattern-recognition problems. I propose that part of the solution relies on a particular architecture that imposes a dynamic format on odour codes. According to this hypothesis, the olfactory system actively creates a large coding space in which to place odour representations and simultaneously optimizes their distribution within it. This process uses both oscillatory and non-periodic dynamic processes with complementary functions: slow non-periodic processes underlie decorrelation, whereas fast oscillations allow sparsening and feature binding.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>12415296</pmid><doi>10.1038/nrn964</doi><tpages>12</tpages></addata></record>
fulltext fulltext
identifier ISSN: 1471-003X
ispartof Nature reviews. Neuroscience, 2002-11, Vol.3 (11), p.884-895
issn 1471-003X
1471-0048
1471-0048
1469-3178
language eng
recordid cdi_proquest_miscellaneous_72643674
source MEDLINE; SpringerLink Journals; Nature
subjects Animal Genetics and Genomics
Animals
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain
Ganglia, Invertebrate - cytology
Ganglia, Invertebrate - physiology
Humans
Hypotheses
Muscular Dystrophy, Animal
Nerve Net - cytology
Nerve Net - physiology
Neurobiology
Neurons
Neurons - physiology
Neurosciences
Olfactory Bulb - cytology
Olfactory Bulb - physiology
Olfactory Pathways - cytology
Olfactory Pathways - physiology
review-article
Signal Transduction - physiology
Smell - physiology
Synaptic Transmission - physiology
title Olfactory network dynamics and the coding of multidimensional signals
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-24T01%3A36%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Olfactory%20network%20dynamics%20and%20the%20coding%20of%20multidimensional%20signals&rft.jtitle=Nature%20reviews.%20Neuroscience&rft.au=Laurent,%20Gilles&rft.date=2002-11-01&rft.volume=3&rft.issue=11&rft.spage=884&rft.epage=895&rft.pages=884-895&rft.issn=1471-003X&rft.eissn=1471-0048&rft_id=info:doi/10.1038/nrn964&rft_dat=%3Cproquest_cross%3E72643674%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=220136243&rft_id=info:pmid/12415296&rfr_iscdi=true