An Anatomically Constrained Model for Path Integration in the Bee Brain

Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odome...

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Vydané v:Current biology Ročník 27; číslo 20; s. 3069
Hlavní autori: Stone, Thomas, Webb, Barbara, Adden, Andrea, Weddig, Nicolai Ben, Honkanen, Anna, Templin, Rachel, Wcislo, William, Scimeca, Luca, Warrant, Eric, Heinze, Stanley
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: England 23.10.2017
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ISSN:1879-0445, 1879-0445
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Abstract Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.
AbstractList Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.
Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.
Author Adden, Andrea
Warrant, Eric
Scimeca, Luca
Webb, Barbara
Wcislo, William
Heinze, Stanley
Stone, Thomas
Weddig, Nicolai Ben
Honkanen, Anna
Templin, Rachel
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  organization: School of Informatics, University of Edinburgh, Edinburgh, UK
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  organization: School of Informatics, University of Edinburgh, Edinburgh, UK
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  surname: Adden
  fullname: Adden, Andrea
  organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden
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  givenname: Nicolai Ben
  surname: Weddig
  fullname: Weddig, Nicolai Ben
  organization: School of Informatics, University of Edinburgh, Edinburgh, UK
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  surname: Honkanen
  fullname: Honkanen, Anna
  organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden
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  organization: Queensland Brain Institute, University of Queensland, Brisbane, Australia
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  organization: Smithsonian Tropical Research Institute, Panama City, Panama
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  fullname: Scimeca, Luca
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  surname: Heinze
  fullname: Heinze, Stanley
  email: stanley.heinze@biol.lu.se
  organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden. Electronic address: stanley.heinze@biol.lu.se
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Issue 20
Keywords optic flow
navigation
compass orientation
polarized light
circuit modeling
insect brain
path integration
central complex
robotics
neuroanatomy
Language English
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  text: 2017-10-23
  day: 23
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PublicationTitle Current biology
PublicationTitleAlternate Curr Biol
PublicationYear 2017
References 29065292 - Curr Biol. 2017 Oct 23;27(20):R1113-R1116. doi: 10.1016/j.cub.2017.09.004.
References_xml – reference: 29065292 - Curr Biol. 2017 Oct 23;27(20):R1113-R1116. doi: 10.1016/j.cub.2017.09.004.
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Snippet Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey,...
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SubjectTerms Animals
Bees
Brain - physiology
Models, Anatomic
Space Perception - physiology
Spatial Navigation - physiology
Title An Anatomically Constrained Model for Path Integration in the Bee Brain
URI https://www.ncbi.nlm.nih.gov/pubmed/28988858
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