An Anatomically Constrained Model for Path Integration in the Bee Brain

Research output: Contribution to journalArticle

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.

Details

Authors
Organisations
External organisations
  • University of Edinburgh
  • University of Queensland
  • Smithsonian Tropical Research Institute
Research areas and keywords

Subject classification (UKÄ) – MANDATORY

  • Zoology
  • Behavioral Sciences Biology

Keywords

  • navigation, path integration, central complex, polarized light, optic flow, circuit modeling, insect brain, robotics, compass orientation, neuroanatomy
Original languageEnglish
Pages (from-to)3069-3085.e11
JournalCurrent Biology
Volume27
Issue number20
Early online date2017 Oct 4
Publication statusPublished - 2017 Oct
Publication categoryResearch
Peer-reviewedYes