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Reactive Searching and Infotaxis in Odor Source Localization

Identifieur interne : 000084 ( Pmc/Curation ); précédent : 000083; suivant : 000085

Reactive Searching and Infotaxis in Odor Source Localization

Auteurs : Nicole Voges [France] ; Antoine Chaffiol [France] ; Philippe Lucas [France] ; Dominique Martinez [France]

Source :

RBID : PMC:4211930

Abstract

Male moths aiming to locate pheromone-releasing females rely on stimulus-adapted search maneuvers complicated by a discontinuous distribution of pheromone patches. They alternate sequences of upwind surge when perceiving the pheromone and cross- or downwind casting when the odor is lost. We compare four search strategies: three reactive versus one cognitive. The former consist of pre-programmed movement sequences triggered by pheromone detections while the latter uses Bayesian inference to build spatial probability maps. Based on the analysis of triphasic responses of antennal lobe neurons (On, inhibition, Off), we propose three reactive strategies. One combines upwind surge (representing the On response to a pheromone detection) and spiral casting, only. The other two additionally include crosswind (zigzag) casting representing the Off phase. As cognitive strategy we use the infotaxis algorithm which was developed for searching in a turbulent medium. Detection events in the electroantennogram of a moth attached to a robot indirectly control this cyborg, depending on the strategy in use. The recorded trajectories are analyzed with regard to success rates, efficiency, and other features. In addition, we qualitatively compare our robotic trajectories to behavioral search paths. Reactive searching is more efficient (yielding shorter trajectories) for higher pheromone doses whereas cognitive searching works better for lower doses. With respect to our experimental conditions (2 m from starting position to pheromone source), reactive searching with crosswind zigzag yields the shortest trajectories (for comparable success rates). Assuming that the neuronal Off response represents a short-term memory, zigzagging is an efficient movement to relocate a recently lost pheromone plume. Accordingly, such reactive strategies offer an interesting alternative to complex cognitive searching.


Url:
DOI: 10.1371/journal.pcbi.1003861
PubMed: 25330317
PubMed Central: 4211930

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PMC:4211930

Le document en format XML

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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS Comput Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Comput. Biol</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">ploscomp</journal-id>
<journal-title-group>
<journal-title>PLoS Computational Biology</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-734X</issn>
<issn pub-type="epub">1553-7358</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25330317</article-id>
<article-id pub-id-type="pmc">4211930</article-id>
<article-id pub-id-type="publisher-id">PCOMPBIOL-D-14-00308</article-id>
<article-id pub-id-type="doi">10.1371/journal.pcbi.1003861</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Biology and Life Sciences</subject>
<subj-group>
<subject>Computational Biology</subject>
<subj-group>
<subject>Computational Neuroscience</subject>
<subj-group>
<subject>Coding Mechanisms</subject>
<subject>Single Neuron Function</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group>
<subject>Neuroscience</subject>
<subj-group>
<subject>Cognitive Science</subject>
<subj-group>
<subject>Cognition</subject>
<subj-group>
<subject>Animal Cognition</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Artificial Intelligence</subject>
<subj-group>
<subject>Machine Learning</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group>
<subject>Sensory Systems</subject>
<subj-group>
<subject>Olfactory System</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Behavioral Neuroscience</subject>
</subj-group>
</subj-group>
<subj-group>
<subject>Systems Biology</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2">
<subject>Computer and Information Sciences</subject>
<subj-group>
<subject>Computerized Simulations</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Reactive Searching and Infotaxis in Odor Source Localization</article-title>
<alt-title alt-title-type="running-head">Reactive Searching and Infotaxis in Odor Source Localization</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Voges</surname>
<given-names>Nicole</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chaffiol</surname>
<given-names>Antoine</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lucas</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Martinez</surname>
<given-names>Dominique</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
<addr-line>CNRS, LORIA, UMR 7503, Vandoeuvre-les-Nancy, France</addr-line>
</aff>
<aff id="aff2">
<label>2</label>
<addr-line>Inserm, UMR S968, Institut de la Vision, Paris, France</addr-line>
</aff>
<aff id="aff3">
<label>3</label>
<addr-line>INRA, UMR 1392, Institute of Ecology and Environmental Sciences of Paris, Versailles, France</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Ayers</surname>
<given-names>Joseph</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Northeastern University, United States of America</addr-line>
</aff>
<author-notes>
<corresp id="cor1">* E-mail:
<email>nicole.voges@gmx.com</email>
</corresp>
<fn fn-type="conflict">
<p>The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con">
<p>Conceived and designed the experiments: NV AC PL DM. Performed the experiments: NV AC PL DM. Analyzed the data: NV AC DM. Contributed reagents/materials/analysis tools: NV AC PL DM. Wrote the paper: NV.</p>
</fn>
<fn id="fn1" fn-type="current-aff">
<label>¤</label>
<p>Current address: CRG, Sensory Systems and Behaviour, Barcelona, Spain</p>
</fn>
</author-notes>
<pub-date pub-type="collection">
<month>10</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>16</day>
<month>10</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="ecorrected">
<day>28</day>
<month>10</month>
<year>2014</year>
</pub-date>
<volume>10</volume>
<issue>10</issue>
<elocation-id>e1003861</elocation-id>
<history>
<date date-type="received">
<day>17</day>
<month>2</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>8</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-year>2014</copyright-year>
<copyright-holder>Voges et al</copyright-holder>
<license>
<license-p>This is an open-access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract>
<p>Male moths aiming to locate pheromone-releasing females rely on stimulus-adapted search maneuvers complicated by a discontinuous distribution of pheromone patches. They alternate sequences of upwind surge when perceiving the pheromone and cross- or downwind casting when the odor is lost. We compare four search strategies: three reactive versus one cognitive. The former consist of pre-programmed movement sequences triggered by pheromone detections while the latter uses Bayesian inference to build spatial probability maps. Based on the analysis of triphasic responses of antennal lobe neurons (On, inhibition, Off), we propose three reactive strategies. One combines upwind surge (representing the On response to a pheromone detection) and spiral casting, only. The other two additionally include crosswind (zigzag) casting representing the Off phase. As cognitive strategy we use the infotaxis algorithm which was developed for searching in a turbulent medium. Detection events in the electroantennogram of a moth attached to a robot indirectly control this cyborg, depending on the strategy in use. The recorded trajectories are analyzed with regard to success rates, efficiency, and other features. In addition, we qualitatively compare our robotic trajectories to behavioral search paths. Reactive searching is more efficient (yielding shorter trajectories) for higher pheromone doses whereas cognitive searching works better for lower doses. With respect to our experimental conditions (2 m from starting position to pheromone source), reactive searching with crosswind zigzag yields the shortest trajectories (for comparable success rates). Assuming that the neuronal Off response represents a short-term memory, zigzagging is an efficient movement to relocate a recently lost pheromone plume. Accordingly, such reactive strategies offer an interesting alternative to complex cognitive searching.</p>
</abstract>
<abstract abstract-type="summary">
<title>Author Summary</title>
<p>The moth mating race is a suitable model case for studying the efficiency of various search strategies and to compare them to real-world behavior. All there is to guide olfactory navigation are simple sporadic clues, i.e., single pheromone detections. Thus, a pheromone seeking male relies on a specifically adapted behavior where action selection is triggered by simple perceptional events. They switch between stereotypical movement sequences, as, for example, upwind surge and crosswind casting. This behavior can be either a consequence of cognitive processing or a reactive reflex of fixed action patterns. Suggesting a direct relationship between neuronal central activity and such action patterns, we combine and implement them as reactive strategies. We also employ infotaxis, an artificial intelligence algorithm specifically developed for searching in turbulent odor plumes. Using these strategies in cyborg experiments, we obtain and compare the resulting search trajectories. Our results indicate that complex, computationally expensive search strategies like infotaxis are not necessarily better than simple reactive ones. With respect to our set-up, reactive searching yields the shortest trajectories if and only if it includes a crosswind zigzagging phase that represents a short-term memory. Thus, already a minimal bit of simplistic memory can produce very efficient goal-directed behavior.</p>
</abstract>
<funding-group>
<funding-statement>This work was funded by the French state program Investissements d'Avenir managed by ANR (grant ANR-10-BINF-05 Pherotaxis). URL:
<ext-link ext-link-type="uri" xlink:href="http://www.agence-nationale-recherche.fr/">http://www.agence-nationale-recherche.fr/</ext-link>
. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts>
<page-count count="13"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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