An Anatomically Constrained Model for Path Integration in the Bee Brain
Open accessAbstract
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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The neural representation of a heading can be maintained even if the fix on the external reference is temporarily lost, enabling insects to maintain a heading and to store vectors of travelled paths in memory.
“The neural representation of that heading can be maintained even if the fix on the external reference is temporarily lost [51,52], which enables insects to maintain a heading and to store vectors of travelled paths in memory [53].”
From Phenomenal interface theory: a model for basal consciousness (2025) · cites this paper as [52]
Both speed and direction parameters are under feedback control, as sensory reafference continuously informs the brain about the body's instantaneous forward velocity and heading.
“Both parameters are also under feedback control, as sensory reafference continuously informs the brain about the body’s instantaneous forward velocity76–78 and heading79”
From Fine-grained descending control of steering in walking Drosophila (2024) · cites this paper as [78]
Both speed and direction parameters are under feedback control, as sensory reafference continuously informs the brain about the body's instantaneous forward velocity and heading.
“Both parameters are also under feedback control, as sensory reafference continuously informs the brain about the body’s instantaneous forward velocity73–75 and heading76.”
From Fine-grained descending control of steering in walking <i>Drosophila</i> (2023) · cites this paper as [75]
World-centric heading direction θ is computed in the ellipsoid body and sent to the protocerebral bridge, while body-centric translation direction φ is relayed to the nodulus.
“Here, world-centric heading direction (θ) is computed in the ellipsoid body and sent to the protocerebral bridge (PB)17–19 while body-centric translation direction (φ) is relayed to the nodulus (NO)20.”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
The central complex is the primary locus of spatial computations in arthropods.
“The central complex is the primary locus of spatial computations in arthropods.”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
In each integrator population, the velocity signal is added to a heading map, and the result is summed over time.
“In each integrator population, this velocity signal is added to a heading map, and the result is summed over time.”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
In the Webb model, each velocity neuron projects to a population of integrator neurons, proposed to be PFN (CPU4) neurons.
“Each velocity neuron projects to a population of “integrator” neurons, proposed to be PFN neurons (also known as CPU4).”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
The Webb model does not contain an explicit representation of world-centric travel velocity; instead, it stores path components separately along two orthogonal axes of translation.
“This model does not contain an explicit representation of world-centric travel velocity; instead, it stores path components separately along two orthogonal axes of translation.”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
The Webb and colleagues model overcomes this limitation with a Cartesian translational velocity system consisting of one neuron tuned to forward-right velocity and another to forward-left velocity.
“A recent model proposed by Webb and colleagues20 overcomes this limitation with a Cartesian system for translational velocity, consisting of one neuron tuned to forward-right velocity, and another neuron tuned to forward-left velocity.”
From Transforming representations of movement from body- to world-centric space (2022) · cites this paper as [20]
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- Authors
- Stone, T., Webb, B., Adden, A., Weddig, N. B., Honkanen, A., Templin, R., Wcislo, W., Scimeca, L., Warrant, E., & Heinze, S.
- Affiliations
- University of Edinburgh (GB)
- Lund University (SE)
- The University of Queensland (AU)
- Smithsonian Tropical Research Institute (PA)
- Corresponding author
- Heinze, Stanley
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2017-10
- Volume
- 27
- Issue
- 20
- Pages
- 3069-3085.e11
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC6196076
- OpenAlex
- W2764135343
- Cited by
- 377
- References
- 73
- Citations by year
- 2026: 36 · 2025: 39 · 2024: 47 · 2023: 56 · 2022: 43 · 2021: 39 · 2020: 38 · 2019: 42 · 2018: 32 · 2017: 3 · 2016: 1 · 2014: 1
- FWCI
- 15.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 387 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cambridge University Engineering Department Publications Database (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by-nc-nd)
- Funders
- Swedish Research Council (621-2012-2213)
- Marie-Curie IntraEuropean Fellowship (327901)
- European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (714599)
- Wenner-Gren Foundation
- Australian Research Foundation
- Air Force Office for Scientific Research
- VR (FA8655-07-C-4011)
- AFOSR (2012-02205)
- Knut and Alice Wallenberg Foundation (KAW 2011.0062, EP/F500385/1, BB/F529254/1)
- University of Edinburgh School of Informatics Doctoral Training Centre in Neuroinformatics and Computational Neuroscience
- UK Engineering and Physical Sciences Research Council (EP/F500385/1)
- UK Biotechnology and Biological Sciences Research Council (BBSRC (BB/F529254/1)
- UK Medical Research Council
- Jennifer and Greg Johnson
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Insect and Arachnid Ecology and Behavior
- Keywords
- path integration, bee navigation, central complex, optical flow, visual odometry, celestial compass, holonomic motion, receptive fields
- MeSH terms
- Animals, Bees, Brain, Models, Anatomic, Space Perception, Spatial Navigation
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