An Anatomically Constrained Model for Path Integration in the Bee Brain

• Published in: Current biology Vol. 27; no. 20; pp. 3069 - 3085.e11
• Main Authors: Stone, Thomas, Webb, Barbara, Adden, Andrea, Weddig, Nicolai Ben, Honkanen, Anna, Templin, Rachel, Wcislo, William, Scimeca, Luca, Warrant, Eric, Heinze, Stanley
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 23.10.2017
• Subjects: Animals; Bees; Behavioral Sciences Biology; Biologi; Biological Sciences; Brain - physiology; central complex; circuit modeling; compass orientation; Etologi; insect brain; Models, Anatomic; Natural Sciences; Naturvetenskap; navigation; neuroanatomy; optic flow; path integration; polarized light; robotics; Space Perception - physiology; Spatial Navigation - physiology; Zoologi; Zoology; optic flow; navigation; polarized light; compass orientation; circuit modeling; insect brain; path integration; central complex; robotics; neuroanatomy
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2017.08.052

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. •Central complex neuroarchitecture suffices as a path integration circuit•Compass heading and forward speed information converge in the bee central complex•Columnar noduli neurons plausibly encode a distributed memory of the home vector•The circuit additionally compares current and desired headings to initiate steering Stone et al. present the first fully biologically constrained model of path integration in the insect brain. This combines newly identified speed and compass neuron convergence with known anatomical features of the central complex and provides a novel functional interpretation of this neuropil’s role across all orientation behaviors.