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 |
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| Hlavní autori: | , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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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. |
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| 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 |
| Author_xml | – sequence: 1 givenname: Thomas surname: Stone fullname: Stone, Thomas organization: School of Informatics, University of Edinburgh, Edinburgh, UK – sequence: 2 givenname: Barbara surname: Webb fullname: Webb, Barbara organization: School of Informatics, University of Edinburgh, Edinburgh, UK – sequence: 3 givenname: Andrea surname: Adden fullname: Adden, Andrea organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden – sequence: 4 givenname: Nicolai Ben surname: Weddig fullname: Weddig, Nicolai Ben organization: School of Informatics, University of Edinburgh, Edinburgh, UK – sequence: 5 givenname: Anna surname: Honkanen fullname: Honkanen, Anna organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden – sequence: 6 givenname: Rachel surname: Templin fullname: Templin, Rachel organization: Queensland Brain Institute, University of Queensland, Brisbane, Australia – sequence: 7 givenname: William surname: Wcislo fullname: Wcislo, William organization: Smithsonian Tropical Research Institute, Panama City, Panama – sequence: 8 givenname: Luca surname: Scimeca fullname: Scimeca, Luca organization: School of Informatics, University of Edinburgh, Edinburgh, UK – sequence: 9 givenname: Eric surname: Warrant fullname: Warrant, Eric organization: Lund Vision Group, Department of Biology, Lund University, Lund, Sweden – sequence: 10 givenname: Stanley 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 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28988858$$D View this record in MEDLINE/PubMed |
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