An Anatomically Constrained Model for Path Integration in the Bee Brain

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An Anatomically Constrained Model for Path Integration in the Bee Brain. / Stone, Thomas; Webb, Barbara; Adden, Andrea; Weddig, Nicolai Ben; Honkanen, Anna; Templin, Rachel; Wcislo, William; Scimeca, Luca; Warrant, Eric; Heinze, Stanley.

I: Current Biology, Vol. 27, Nr. 20, 10.2017, s. 3069-3085.e11.

Forskningsoutput: TidskriftsbidragArtikel i vetenskaplig tidskrift

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Stone, Thomas ; Webb, Barbara ; Adden, Andrea ; Weddig, Nicolai Ben ; Honkanen, Anna ; Templin, Rachel ; Wcislo, William ; Scimeca, Luca ; Warrant, Eric ; Heinze, Stanley. / An Anatomically Constrained Model for Path Integration in the Bee Brain. I: Current Biology. 2017 ; Vol. 27, Nr. 20. s. 3069-3085.e11.

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TY - JOUR

T1 - An Anatomically Constrained Model for Path Integration in the Bee Brain

AU - Stone, Thomas

AU - Webb, Barbara

AU - Adden, Andrea

AU - Weddig, Nicolai Ben

AU - Honkanen, Anna

AU - Templin, Rachel

AU - Wcislo, William

AU - Scimeca, Luca

AU - Warrant, Eric

AU - Heinze, Stanley

N1 - Copyright © 2017 Elsevier Ltd. All rights reserved.

PY - 2017/10

Y1 - 2017/10

N2 - 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.

AB - 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.

KW - navigation

KW - path integration

KW - central complex

KW - polarized light

KW - optic flow

KW - circuit modeling

KW - insect brain

KW - robotics

KW - compass orientation

KW - neuroanatomy

U2 - 10.1016/j.cub.2017.08.052

DO - 10.1016/j.cub.2017.08.052

M3 - Article

VL - 27

SP - 3069-3085.e11

JO - Current Biology

JF - Current Biology

SN - 1879-0445

IS - 20

ER -