A Neural Network for Wind-Guided Compass Navigation

Okubo, Tatsuo S.; Patella, Paola; D’Alessandro, Isabel; Wilson, Rachel I.

doi:10.1016/j.neuron.2020.06.022

Cited by 116Neurobiology and Insect Physiology ResearchMemory and Neural MechanismsSpatial Cognition and Navigation

A Neural Network for Wind-Guided Compass Navigation

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Okubo, Tatsuo S., Patella, Paola, D’Alessandro, Isabel, Wilson, Rachel I.·2020·Neuron

DOI 10.1016/j.neuron.2020.06.022PMC PMC7507644

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Abstract

Spatial maps in the brain are most accurate when they are linked to external sensory cues. Here, we show that the compass in the Drosophila brain is linked to the direction of the wind. Shifting the wind rightward rotates the compass as if the fly were turning leftward, and vice versa. We describe the mechanisms of several computations that integrate wind information into the compass. First, an intensity-invariant representation of wind direction is computed by comparing left-right mechanosensory signals. Then, signals are reformatted to reduce the coding biases inherent in peripheral mechanics, and wind cues are brought into the same circular coordinate system that represents visual cues and self-motion signals. Because the compass incorporates both mechanosensory and visual cues, it should enable navigation under conditions where no single cue is consistently reliable. These results show how local sensory signals can be transformed into a global, multimodal, abstract representation of space.

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Ring neurons cluster into different types that encode the position of different orientation cues.
“Ring neurons also cluster into different types which seem to encode the position of different orientation cues [15,17].”
From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [17]
The Discussion (‘R neurons connect the compass to the sensory environment’; page unavailable) reports 11 morphological R-neuron types and says characterized R neurons encode sensory cues related to the fly’s angular position. It specifically finds that both R1 and R3a encode wind direction, but does not establish that different types encode different kinds of orientation cue. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Visual and mechanosensory cues reach the ring neurons in flies, and visual input is confirmed in dung beetles.
“Both visual and mechanosensory cues are known to reach the ring neurons in flies [17], with visual input also being confirmed in dung beetles [27].”
From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [17]
Hebbian learning is often suggested for the construction of R→E-PG mappings.
“Hebbian learning is often suggested for the construction of R → E-PG mappings [16,17,19,20,28,41]).”
From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [17]
None of the individual elements in the model presented are new.
“Conceptually, none of the individual elements in the model we present are new [8,13,17,21,41].”
From A model of cue integration as vector summation in the insect brain (2023) · cites this paper as [17]
The Results section describes this paper’s model of how wind signals reach compass neurons, providing a possible precedent for an element of the citing authors’ model. But the citing sentence does not identify its individual elements, and no passage in our copy establishes that all of them were already known. I searched the modeling results and discussion for a statement about the novelty of those elements. (LLM, conf=0.72)
Experimental — accuracy not yet measured

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Whole-brain annotation and multi-connectome cell typing of Drosophila
Schlegel, P., Yin, Y., Bates, A. S., Dorkenwald, S., Eichler, K., Brooks, P., Han, D. S., Gkantia, M., dos Santos, M., Munnelly, E. J., et al. (2024) · Nature · doi:10.1038/s41586-024-07686-5 · Cited by 413 · see citing works
“However, the adult fly has richer behaviour, including complex motor control while walking or in flight 7 , courtship behaviour 8 , involved decision making 9 , flexible associative memory 10,11 , spatial learning 12 and complex 13,14 multisensory 15,16 navigation.”
Background
A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection
Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2021) · eLife · doi:10.7554/elife.66039 · Cited by 392 · see citing works
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Self-citation
A neural circuit for wind-guided olfactory navigation
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A visual pathway for skylight polarization processing in Drosophila
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Converting an allocentric goal into an egocentric steering signal
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Whole-brain annotation and multi-connectome cell typing quantifies circuit stereotypy in Drosophila
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Open-source tools for behavioral video analysis: Setup, methods, and best practices
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Flexible navigational computations in the Drosophila central complex
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Flight-Induced Compass Representation in the Monarch Butterfly Heading Network
Beetz, M. J., Kraus, C. M., Franzke, M., Dreyer, D., Strube-Bloss, M. F., Rößler, W., Warrant, E. J., Merlin, C., & el Jundi, B. (2021) · Current Biology · doi:10.1016/j.cub.2021.11.009 · Cited by 73 · see citing works
Dopamine promotes head direction plasticity during orienting movements
Fisher, Y. E., Marquis, M., D’Alessandro, I., & Wilson, R. I. (2022) · Nature · doi:10.1038/s41586-022-05485-4 · Cited by 67 · see citing works
Self-citation
How Dung Beetles Steer Straight
Dacke, M., Baird, E., el Jundi, B., Warrant, E. J., & Byrne, M. J. (2020) · Annual Review of Entomology · doi:10.1146/annurev-ento-042020-102149 · Cited by 75 · see citing works
A projectome of the bumblebee central complex
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Emergent behaviour and neural dynamics in artificial agents tracking odour plumes
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“First, agent head direction has been found to be implemented as a ring attractor circuit in the central complex of many flying insects and is implicated in navigation 61–64 .”
Background
Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons
Currier, T. A., Matheson, A. M. M., & Nagel, K. I. (2020) · eLife · doi:10.7554/elife.61510 · Cited by 60 · see citing works
A unified mechanism for innate and learned visual landmark guidance in the insect central complex
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Connectomics and the neural basis of behaviour
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A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection
Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D. B., Takemura, S., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2020) · doi:10.1101/2020.12.08.413955 · Cited by 392 · see citing works
“Besides visual cues, mechanosensory wind stimuli can drive the fly’s head direction system in the EB (Okubo et al., 2020) (Figure 9, Figure 66B).”
BackgroundInfluential
A rise-to-threshold process for a relative-value decision
Vijayan, V., Wang, F., Wang, K., Chakravorty, A., Adachi, A., Akhlaghpour, H., Dickson, B. J., & Maimon, G. (2023) · Nature · doi:10.1038/s41586-023-06271-6 · Cited by 49 · see citing works
Connectomic reconstruction predicts visual features used for navigation
Garner, D., Kind, E., Lai, J. Y. H., Nern, A., Zhao, A., Houghton, L., Sancer, G., Wolff, T., Rubin, G. M., Wernet, M. F., et al. (2024) · Nature · doi:10.1038/s41586-024-07967-z · Cited by 44 · see citing works
Olfactory navigation in arthropods
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The neuronal building blocks of the navigational toolkit in the central complex of insects
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Neural networks for navigation: From connections to computations
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A neural circuit architecture for rapid learning in goal-directed navigation
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Neural circuit mechanisms for transforming learned olfactory valences into wind-oriented movement
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Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex
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How the insect central complex could coordinate multimodal navigation
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Wind gates olfaction-driven search states in free flight
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The sky compass network in the brain of the desert locust
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Neural circuits for goal-directed navigation across species
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The neuroethology of ant navigation
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Active antennal movements in Drosophila can tune wind encoding
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Variations on an ancient theme — the central complex across insects
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Johnston's organ and its central projections in Cataglyphis desert ants
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Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement
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A neuronal substrate for translating nutrient state and resource density estimations into foraging decisionsPreprint
Goldschmidt, D., Tastekin, I., Münch, D., Park, J.-Y., Haberkern, H., Serra, L., Baltazar, C., Jayaraman, V., Rubin, G. M., & Ribeiro, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.19.549514 · Cited by 27 · see citing works
Towards a common terminology for arthropod spatial orientation
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Emergent spatial goals in an integrative model of the insect central complex
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A rotational velocity estimate constructed through visuomotor competition updates the fly’s neural compassPreprint
Hulse, B. K., Stanoev, A., Turner‐Evans, D. B., Seelig, J. D., & Jayaraman, V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.25.559373 · Cited by 20 · see citing works
Maintaining a stable head direction representation in naturalistic visual environments
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Sensorimotor ecology of the insect antenna: Active sampling by a multimodal sensory organ
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Dynamic antennal positioning allows honeybee followers to decode the dance
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A neural circuit architecture for rapid behavioral flexibility in goal-directed navigation
Dan, C., Hulse, B. K., Kappagantula, R., Jayaraman, V., & Hermundstad, A. M. (2021) · doi:10.1101/2021.08.18.456004 · Cited by 51 · see citing works
Weighting of Celestial and Terrestrial Cues in the Monarch Butterfly Central Complex
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A three‐dimensional atlas of the honeybee central complex, associated neuropils and peptidergic layers of the central body
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Behavioral algorithms and neural mechanisms underlying odor-modulated locomotion in insects
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Interactions between specialized gain control mechanisms in olfactory processing
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A model of cue integration as vector summation in the insect brain
Mitchell, R., Shaverdian, S., Dacke, M., & Webb, B. (2023) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2023.0767 · Cited by 13 · see citing works
3D‐atlas of the brain of the cockroach Rhyparobia maderae
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Integration of sleep homeostasis and navigation in Drosophila
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Mechanosensory Stimulation via Nanchung Expressing Neurons Can Induce Daytime Sleep in Drosophila
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Performance of polarization-sensitive neurons of the locust central complex at different degrees of polarization
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Thermoresponsive motor behavior is mediated by ring neuron circuits in the central complex of Drosophila
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Sexual dimorphism in the complete Drosophila male central nervous system connectome
Berg, S., Beckett, I. R., Costa, M., Philipp, S., Januszewski, M., Marin, E. C., Nern, A., Preibisch, S., Qiu, W., Takemura, S.-Y., et al. (2026) · Cell · doi:10.1016/j.cell.2026.08.015 · Cited by 68 · see citing works
Integration of optic flow into the sky compass network in the brain of the desert locust
Zittrell, F., Pabst, K., Carlomagno, E., Rosner, R., Pegel, U., Endres, D., & Homberg, U. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1111310 · Cited by 14 · see citing works
Organization and neural connections of the lateral complex in the brain of the desert locust
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Neuronal calcium spikes enable vector inversion in the Drosophila brain
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Insect Orientation: The Drosophila Wind Compass Pathway
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Multimodal cue integration and learning in a neural representation of head direction
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“The bump’s position changes smoothly as the fly rotates, reflecting the influence of self-motion cues 37,38 and external sensory inputs 34,39 (Fig.”
Self-citation
3D atlas of cerebral neuropils with previously unknown demarcations in the honey bee brain
Habenstein, J., Grübel, K., Pfeiffer, K., & Rößler, W. (2023) · The Journal of Comparative Neurology · doi:10.1002/cne.25486 · Cited by 12 · see citing works
STPoseNet: A real-time spatiotemporal network model for robust mouse pose estimation
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A neural circuit for wind-guided olfactory navigationPreprint
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Self-citation

Authors: Okubo, T. S., Patella, P., D’Alessandro, I., & Wilson, R. I.
Affiliations: Harvard University (US)
Corresponding author: Wilson, Rachel I.
ORCID: Okubo, Tatsuo S.
Patella, Paola
D’Alessandro, Isabel
Wilson, Rachel I.
Venue: Neuron
Publisher: Elsevier BV
Published: 2020-09
Volume: 107
Issue: 5
Pages: 924-940.e18
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2020.06.022
PMC: PMC7507644
OpenAlex: W3043725759
Cited by: 114
References: 120
Citations by year: 2026: 9 · 2025: 16 · 2024: 20 · 2023: 23 · 2022: 24 · 2021: 18 · 2020: 4
FWCI: 7.86
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, 373 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
Keywords: Drosophila, wind direction, visual cues, self-motion signals, spatial maps, multimodal integration, neural network model
MeSH terms: Animals, Brain, Cues, Drosophila melanogaster, Mechanoreceptors, Nerve Net, Neurons, Wind, Arthropod Antennae, Spatial Navigation

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A Neural Network for Wind-Guided Compass Navigation

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