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An Anatomically Constrained Model for Path Integration in the Bee Brain

Stone, Thomas; Webb, Barbara; Adden, Andrea LU ; Weddig, Nicolai Ben; Honkanen, Anna LU ; Templin, Rachel; Wcislo, William; Scimeca, Luca; Warrant, Eric LU and Heinze, Stanley LU (2017) In Current Biology
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... (More)

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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Please use this url to cite or link to this publication:
author
organization
publishing date
type
Contribution to journal
publication status
epub
subject
keywords
navigation, path integration, central complex, polarized light, optic flow, circuit modeling, insect brain, robotics, compass orientation, neuroanatomy
in
Current Biology
publisher
Elsevier
external identifiers
  • scopus:85030181191
  • wos:000413441700019
ISSN
1879-0445
DOI
10.1016/j.cub.2017.08.052
language
English
LU publication?
yes
id
0595256e-d8f0-42a1-b397-45b2a56153ea
date added to LUP
2017-10-13 16:33:18
date last changed
2018-01-16 13:22:58
@article{0595256e-d8f0-42a1-b397-45b2a56153ea,
  abstract     = {<p>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.</p>},
  author       = {Stone, Thomas and Webb, Barbara and Adden, Andrea and Weddig, Nicolai Ben and Honkanen, Anna and Templin, Rachel and Wcislo, William and Scimeca, Luca and Warrant, Eric and Heinze, Stanley},
  issn         = {1879-0445},
  keyword      = {navigation,path integration,central complex,polarized light,optic flow,circuit modeling,insect brain,robotics,compass orientation,neuroanatomy},
  language     = {eng},
  month        = {10},
  publisher    = {Elsevier},
  series       = {Current Biology},
  title        = {An Anatomically Constrained Model for Path Integration in the Bee Brain},
  url          = {http://dx.doi.org/10.1016/j.cub.2017.08.052},
  year         = {2017},
}