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Curr Biol. 2017 Oct 23;27(20):3069-3085.e11. doi: 10.1016/j.cub.2017.08.052. Epub 2017 Oct 5.

An Anatomically Constrained Model for Path Integration in the Bee Brain.

Author information

1
School of Informatics, University of Edinburgh, Edinburgh, UK.
2
Lund Vision Group, Department of Biology, Lund University, Lund, Sweden.
3
Queensland Brain Institute, University of Queensland, Brisbane, Australia.
4
Smithsonian Tropical Research Institute, Panama City, Panama.
5
Lund Vision Group, Department of Biology, Lund University, Lund, Sweden. Electronic address: stanley.heinze@biol.lu.se.

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.

KEYWORDS:

central complex; circuit modeling; compass orientation; insect brain; navigation; neuroanatomy; optic flow; path integration; polarized light; robotics

PMID:
28988858
PMCID:
PMC6196076
DOI:
10.1016/j.cub.2017.08.052
[Indexed for MEDLINE]
Free PMC Article

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