Decentralized Multisensory Information Integration in Neural Systems
Identifieur interne : 000121 ( Pmc/Curation ); précédent : 000120; suivant : 000122Decentralized Multisensory Information Integration in Neural Systems
Auteurs : Wen-Hao Zhang [République populaire de Chine] ; Aihua Chen [République populaire de Chine] ; Malte J. Rasch [République populaire de Chine] ; Si Wu [République populaire de Chine]Source :
- The Journal of Neuroscience [ 0270-6474 ] ; 2016.
Abstract
How multiple sensory cues are integrated in neural circuitry remains a challenge. The common hypothesis is that information integration might be accomplished in a dedicated multisensory integration area receiving feedforward inputs from the modalities. However, recent experimental evidence suggests that it is not a single multisensory brain area, but rather many multisensory brain areas that are simultaneously involved in the integration of information. Why many mutually connected areas should be needed for information integration is puzzling. Here, we investigated theoretically how information integration could be achieved in a distributed fashion within a network of interconnected multisensory areas. Using biologically realistic neural network models, we developed a decentralized information integration system that comprises multiple interconnected integration areas. Studying an example of combining visual and vestibular cues to infer heading direction, we show that such a decentralized system is in good agreement with anatomical evidence and experimental observations. In particular, we show that this decentralized system can integrate information optimally. The decentralized system predicts that optimally integrated information should emerge locally from the dynamics of the communication between brain areas and sheds new light on the interpretation of the connectivity between multisensory brain areas.
Url:
DOI: 10.1523/JNEUROSCI.0578-15.2016
PubMed: 26758843
PubMed Central: 4710773
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<front><div type="abstract" xml:lang="en"><p>How multiple sensory cues are integrated in neural circuitry remains a challenge. The common hypothesis is that information integration might be accomplished in a dedicated multisensory integration area receiving feedforward inputs from the modalities. However, recent experimental evidence suggests that it is not a single multisensory brain area, but rather many multisensory brain areas that are simultaneously involved in the integration of information. Why many mutually connected areas should be needed for information integration is puzzling. Here, we investigated theoretically how information integration could be achieved in a distributed fashion within a network of interconnected multisensory areas. Using biologically realistic neural network models, we developed a decentralized information integration system that comprises multiple interconnected integration areas. Studying an example of combining visual and vestibular cues to infer heading direction, we show that such a decentralized system is in good agreement with anatomical evidence and experimental observations. In particular, we show that this decentralized system can integrate information optimally. The decentralized system predicts that optimally integrated information should emerge locally from the dynamics of the communication between brain areas and sheds new light on the interpretation of the connectivity between multisensory brain areas.</p>
<p><bold>SIGNIFICANCE STATEMENT</bold>
To extract information reliably from ambiguous environments, the brain integrates multiple sensory cues, which provide different aspects of information about the same entity of interest. Here, we propose a decentralized architecture for multisensory integration. In such a system, no processor is in the center of the network topology and information integration is achieved in a distributed manner through reciprocally connected local processors. Through studying the inference of heading direction with visual and vestibular cues, we show that the decentralized system can integrate information optimally, with the reciprocal connections between processers determining the extent of cue integration. Our model reproduces known multisensory integration behaviors observed in experiments and sheds new light on our understanding of how information is integrated in the brain.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Neurosci</journal-id>
<journal-id journal-id-type="hwp">jneuro</journal-id>
<journal-id journal-id-type="pmc">jneurosci</journal-id>
<journal-id journal-id-type="publisher-id">J. Neurosci</journal-id>
<journal-title-group><journal-title>The Journal of Neuroscience</journal-title>
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<issn pub-type="ppub">0270-6474</issn>
<issn pub-type="epub">1529-2401</issn>
<publisher><publisher-name>Society for Neuroscience</publisher-name>
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<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
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<title-group><article-title>Decentralized Multisensory Information Integration in Neural Systems</article-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Wen-hao</given-names>
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<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-7641-5024</contrib-id>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
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<xref ref-type="aff" rid="aff2"><sup>2</sup>
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<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Aihua</given-names>
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<xref ref-type="aff" rid="aff3"><sup>3</sup>
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<contrib contrib-type="author" corresp="yes"><name><surname>Rasch</surname>
<given-names>Malte J.</given-names>
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<xref ref-type="aff" rid="aff2"><sup>2</sup>
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<contrib contrib-type="author" corresp="yes"><name><surname>Wu</surname>
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<xref ref-type="aff" rid="aff2"><sup>2</sup>
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<aff id="aff1"><sup>1</sup>
Institute of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China,</aff>
<aff id="aff2"><sup>2</sup>
State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China, and</aff>
<aff id="aff3"><sup>3</sup>
Key Laboratory of Brain Functional Genomics, Primate Research Center, East China Normal University, Shanghai 200062, China</aff>
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<author-notes><corresp>Correspondence should be addressed to either Si Wu or Malte Rasch,
<addr-line>State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China,</addr-line>
<email>wusi@bnu.edu.cn</email>
or <email>malte.rasch@bnu.edu.cn</email>
</corresp>
<fn fn-type="con"><p>Author contributions: W.Z. and S.W. designed research; W.Z. and S.W. performed research; W.Z., A.C., M.J.R., and S.W. analyzed data; W.Z., M.J.R., and S.W. wrote the paper.</p>
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<pub-date pub-type="ppub"><day>13</day>
<month>1</month>
<year>2016</year>
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<month>1</month>
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<volume>36</volume>
<issue>2</issue>
<fpage>532</fpage>
<lpage>547</lpage>
<history><date date-type="received"><day>10</day>
<month>2</month>
<year>2015</year>
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<date date-type="rev-recd"><day>10</day>
<month>11</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>19</day>
<month>11</month>
<year>2015</year>
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<permissions><copyright-statement>Copyright © 2016 Zhang et al.</copyright-statement>
<copyright-year>2016</copyright-year>
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<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="zns00216000532.pdf"></self-uri>
<abstract><p>How multiple sensory cues are integrated in neural circuitry remains a challenge. The common hypothesis is that information integration might be accomplished in a dedicated multisensory integration area receiving feedforward inputs from the modalities. However, recent experimental evidence suggests that it is not a single multisensory brain area, but rather many multisensory brain areas that are simultaneously involved in the integration of information. Why many mutually connected areas should be needed for information integration is puzzling. Here, we investigated theoretically how information integration could be achieved in a distributed fashion within a network of interconnected multisensory areas. Using biologically realistic neural network models, we developed a decentralized information integration system that comprises multiple interconnected integration areas. Studying an example of combining visual and vestibular cues to infer heading direction, we show that such a decentralized system is in good agreement with anatomical evidence and experimental observations. In particular, we show that this decentralized system can integrate information optimally. The decentralized system predicts that optimally integrated information should emerge locally from the dynamics of the communication between brain areas and sheds new light on the interpretation of the connectivity between multisensory brain areas.</p>
<p><bold>SIGNIFICANCE STATEMENT</bold>
To extract information reliably from ambiguous environments, the brain integrates multiple sensory cues, which provide different aspects of information about the same entity of interest. Here, we propose a decentralized architecture for multisensory integration. In such a system, no processor is in the center of the network topology and information integration is achieved in a distributed manner through reciprocally connected local processors. Through studying the inference of heading direction with visual and vestibular cues, we show that the decentralized system can integrate information optimally, with the reciprocal connections between processers determining the extent of cue integration. Our model reproduces known multisensory integration behaviors observed in experiments and sheds new light on our understanding of how information is integrated in the brain.</p>
</abstract>
<kwd-group><kwd>continuous attractor neural network</kwd>
<kwd>decentralized information integration</kwd>
</kwd-group>
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