The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.
A neural circuit architecture for angular integration in Drosophila
Open accessAbstract
Many animals keep track of their angular heading over time while navigating through their environment. However, a neural-circuit architecture for computing heading has not been experimentally defined in any species. Here we describe a set of clockwise- and anticlockwise-shifting neurons in the Drosophila central complex whose wiring and physiology provide a means to rotate an angular heading estimate based on the fly's angular velocity. We show that each class of shifting neurons exists in two subtypes, with spatiotemporal activity profiles that suggest different roles for each subtype at the start and end of tethered-walking turns. Shifting neurons are required for the heading system to properly track the fly's heading in the dark, and stimulation of these neurons induces predictable shifts in the heading signal. The central features of this biological circuit are analogous to those of computational models proposed for head-direction cells in rodents and may shed light on how neural systems, in general, perform integration.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“No statistical methods were used to predetermine sample sizes but our sample sizes are similar to those reported in previous publications23,24,33,34,37,38.”
From Multimodal cue integration and learning in a neural representation of head direction (2025) · cites this paper as [38]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Similarly, compartments of PEN2 neurons in the protocerebral bridge have been shown to respond entirely differently from their compartments in the ellipsoid body (Green et al., 2017; Turner-Evans et al., 2019).”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Green et al., 2017
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Another well studied neuropil, the EB, is known to be involved in navigation, supporting persistent activity correlated to heading direction57–59.”
From Network statistics of the whole-brain connectome of Drosophila (2024) · cites this paper as [58]
In the citing paper
“we found that there is a single bump of activity in the EPG ensemble whose angular velocity generally correlates with the fly’s angular velocity (Green et al., 2017; Seelig and Jayaraman, 2015; Turner-Evans et al., 2017).”
From Neural circuit mechanisms for steering control in walking Drosophila (2025) · cites this paper as Green et al., 2017
In the citing paper
“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 [19]
In the citing paper
“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 [19]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Ultrasensitive fluorescent proteins for imaging neuronal activity
Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., et al. (2013) · Nature · doi:10.1038/nature12354 · Cited by 6,474
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068
The Dance Language and Orientation of Bees
von Frisch, K. (1993) · Harvard University Press eBooks · doi:10.4159/harvard.9780674418776 · Cited by 2,585
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809
Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex
Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M.-B., & Moser, E. I. (2006) · Science · doi:10.1126/science.1125572 · Cited by 1,485
Sensitive red protein calcium indicators for imaging neural activity
Dana, H., Mohar, B., Sun, Y., Narayan, S., Gordus, A. G., Hasseman, J. P., Tsegaye, G., Holt, G. T., Hu, A., Walpita, D., et al. (2016) · eLife · doi:10.7554/elife.12727 · Cited by 1,055
Zhang, K. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02112.1996 · Cited by 1,001
The Head Direction Signal: Origins and Sensory-Motor Integration
Taube, J. S. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112854 · Cited by 969
Flagged first, then by citations
Research works printed but not linked: 1
- Wehner, R. & Srinivasan, M. in The Neurobiology of Spatial Behaviour (ed. Jeffery, K. J. ) Ch. 1 (Oxford Univ. Press, 2003)
Cited by
Sorted by citations
Items 301–336 of 336
A historical perspective on the insect central complex: Anatomy, development, and function
Gillet, V., Kluge, J., & Patel, R. N. (2023) · Molecular Psychology Brain Behavior and Society · doi:10.12688/molpsychol.17564.1
How mantis shrimp compound eye recognizes circularly polarized lightPreprint
Lou, F., Qu, X., Schunter, C., Wang, L., Tang, Y., Han, Z., & Kang, B. (2023) · doi:10.22541/au.169339743.30080820/v1
Bio-inspired circular latent spaces to estimate objects' rotations
Plebe, A., & Lio, M. D. (2023) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2023.1268116
Non-symbolic estimation of big and small ratios with accurate and noisy feedback
Morton, N. J., Grice, M., Kemp, S. P. T., & Grace, R. C. (2024) · Attention Perception & Psychophysics · doi:10.3758/s13414-024-02914-6
“The neural circuitry supporting path integration is an active area of research in insect neuroscience (e.g., Green et al., 2017, 2019; Lyu et al., 2022).”
BackgroundNormative approaches to neural coding and behavior
Hermundstad, A. M. (2024) · SciPost Physics Lecture Notes · doi:10.21468/scipostphyslectnotes.83
“A population of “compass neurons” maintains a persistent bump of activity that encodes the fly’s current heading [ 63 ] , and that can be updated by integrating the fly’s angular velocity [ 61, 64 ] (Figure 12).”
BackgroundPolarization Sensitivity in the Vinegar Fly, Drosophila melanogaster
Puisais, S. M., Simdianova, A., & Wernet, M. F. (2024) · Springer series in vision research · doi:10.1007/978-3-031-62863-4_1
Continuous integration of heading and goal directions guides steeringPreprint
Crown, A. M., Wu, A. H., Hofflander, L., & Barnea, G. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.24.620060
From the fly connectome to exact ring attractor dynamicsPreprint
Tirthabir Biswas, A., Stanoev, A., Romani, S., & Fitzgerald, J. E. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.01.621596
Wolff, T., Eddison, M., Chen, N., Nern, A., Sundaramurthi, P., Sitaraman, D., & Rubin, G. M. (2025) · eLife · doi:10.7554/elife.104764.1
Taube, J. S., Butler, W. N., Dumont, J. R., Graham, J. A., Marcroft, J. L., Shinder, M. E., Stackman, R. W., & Yoder, R. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.11.648409
Claudi, F., Chandra, S., & Fiete, I. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.07.652608
“…specialized to represent and integrate continuous variables (Figure 1A) [1, 2]: the head direction circuits in mammals [3, 4, 5], fish [6], and flies [7, 8, 9, 10], the oculomotor system of vertebrates [11, 12, 13, 14, 15], and grid cell networks in mammals [16, 17, 18] (see Figure 1B,C,D).”
Chen, Z., & Wang, H. (2025) · Sensors · doi:10.3390/s25113540
“Recent advances in neuroscience have further illuminated the neural circuits underlying coordinate transformations [11,24], providing valuable insights into neuroscience and computing.”
Claudi, F., Chandra, S., & Fiete, I. (2025) · eLife · doi:10.7554/elife.107224
Behery, D. G., Green, D. M., Klimczyk, V. H., Pigin, M., & Keinath, A. T. (2025) · iScience · doi:10.1016/j.isci.2025.113602
Composing trajectories for rapid inference of navigational goals
Abdelrahman, N. Y., Jiang, W.-C., Coddington, L. T., Gong, S., Dudman, J. T., & Hermundstad, A. M. (2026) · Neuron · doi:10.1016/j.neuron.2026.05.030 · Cited by 4
Split-trial analysis reveals the information capacity of neural population codesPreprint
Le, D., & Wei, X.-X. (2025) · eLife · doi:10.1101/2025.11.27.690979
Deep evolution and conserved brain circuitry across bilaterian animals
Hirth, F., & Strausfeld, N. J. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00035-x
Vector coordinate transformation in the Drosophila navigation systemPreprint
Gorko, B., & Kim, S. S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.20.695733
Divergent excitatory and inhibitory signaling in a head direction circuitPreprint
Eddy, J., Shenasa, A. H., Alfaro, P. M., Viveros, M. F., & Turner‐Evans, D. B. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.18.700161 · Cited by 1
Developmental temporal programs govern and maintain neuronal identity and function in adult circuitsPreprint
Wani, A. R., Ashraf, R., Woerner, R. K. R., Marriner, Z., Velasquez, M., Azam, T., Joo, Q. B., Dus, M., & Syed, M. H. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.28.702037
Egocentric Head Direction Encoding and Perception Model Based on an Adaptive Ring Attractor Network
Chen, Z., Wang, H., Li, J., Li, G., & Wang, S. (2026) · IEEE Transactions on Neural Networks and Learning Systems · doi:10.1109/tnnls.2026.3656687
“M ANY animals, such as mammals [1] and insects [2], that can navigate to their home and forage for food in a spatial environment, extensively rely on their spatial cognitive skills [3], [4].”
A multi-resolution imaging and analysis pipeline for comparative circuit reconstruction in insectsPreprint
Gillet, V., Sayre, M. E., Badalamente, G. S., Schieber, N. L., Tedore, K., Funke, J., & Heinze, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.25.708065 · Cited by 1
What Are the Contributions of Modeling to Bridging the Gaps between Methods and across Species?
Bičanski, A. (2026) · Springer eBooks · doi:10.1007/978-3-032-20563-6_5
Visual navigation in ants : a modelling approach
Moël, F. L. (2021) · theses.fr (ABES) · doi:10.70675/3026bd7czd4f4z4419zb4a4ze91e077117ed
A multi-resolution imaging and analysis pipeline for comparative circuit reconstruction in insectsPreprint
Gillet, V., Sayre, M. E., Badalamente, G. S., Schieber, N. L., Tedore, K., Funke, J., & Heinze, S. (2026) · eLife · doi:10.7554/elife.110789.1
A disynaptic pathway linking the cerebellum to the hippocampus
Zenelaj, X. (2024) · theses.fr (ABES) · doi:10.70675/94d94e26z34bez4c6bz880az1e3421294c0a
Flight in the dark: different responses to darkness in flying insects
Maya, R., Lerner, N., Karov, B., Tsory, N., Terrile, R., Peleg, O., & Beatus, T. (2026) · Journal of Experimental Biology · doi:10.1242/jeb.251675
Coherence-incoherence patterns in coupled excitable systems
Franović, I., Eydam, S., Zhu, J., Игоревна, С. Н., Costa, F. P., & Schöll, E. (2026) · Physics of Life Reviews · doi:10.1016/j.plrev.2026.07.003 · Cited by 1
Deep conservation of head direction circuits in bees, ants and fliesPreprint
Sayre, M. E., Gillet, V., Ceberg, N., Badalamente, G. S., Pinzon-Rodriguez, A., Griggs, N., Capdevila, L. S., Roberts, R. J. V., Gunnarsson, E. S., Szadaj, F., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.26.740564
Combining sampling and attractor dynamics in spiking models of head direction systems
Pjanovic, V., Zavatone-Veth, J. A., Masset, P., Keemink, S. W., & Nardin, M. (2026) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1014577 · Cited by 1
“The network maintains a good HD estimate for a period of time but slowly loses the true orientation as the various sources of noise accumulate, reminiscent of biological studies [2,42].”
Flies evolved a gyrocompass to maintain navigational accuracy during rapid flight maneuversPreprint
Ros, I. G., Wang, R., Omoto, J. J., Dickson, W. B., & Dickinson, M. H. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.18.744964
“As a result of this circuitry, idiothetic signals encoding clockwise rotation of the fly cause a counterclockwise movement of the EPG activity bump and vice versa 35,36 .”
Matyukhin, V. (2026) · Research Square · doi:10.21203/rs.3.rs-10982367/v1
Wang, Y., Hu, J., Xu, S., Xu, X., Pan, X., & Wang, R. (2026) · Neural Networks · doi:10.1016/j.neunet.2026.109666
Beyond static perception: Animals, neurons and synapses move to compute efficiently
Juusola, M., Takalo, J., Kemppainen, J., MaBouDi, H., Bu, B. Y., Shukla, S., Zhou, Y., Lazar, A. A., & de Polavieja, G. G. (2026) · Physics of Life Reviews · doi:10.1016/j.plrev.2026.09.009 · Cited by 1
A split attractor design for rapidly writing a navigational goal
Lanz, A. J., Kathman, N. D., Hao, E., Ermentrout, B., & Nagel, K. I. (2026) · Nature · doi:10.1038/s41586-026-11144-9 · Cited by 6
Selective control of course correction over long timescales in the Drosophila central complex
Crown, A. M., Wu, A. H., Hofflander, L., & Barnea, G. (2026) · Current Biology · doi:10.1016/j.cub.2026.09.069
Metadata
- Authors
- Green, J., Adachi, A., Shah, K. K., Hirokawa, J. D., Magani, P. S., & Maimon, G.
- Affiliations
- Rockefeller University (US)
- Corresponding author
- Maimon, Gaby
- Venue
- Nature
- Published
- 2017-05-22
- Volume
- 546
- Issue
- 7656
- Pages
- 101-106
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6320684
- OpenAlex
- W2614915054
- Cited by
- 331
- References
- 43
- Citations by year
- 2026: 24 · 2025: 41 · 2024: 39 · 2023: 39 · 2022: 37 · 2021: 30 · 2020: 31 · 2019: 41 · 2018: 31 · 2017: 17
- FWCI
- 16.20
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute for Health and Care Research
- National Institutes of Health (P40OD018537)
- National Institute on Drug Abuse (DP2DA035148)
- National Institute of Neurological Disorders and Stroke (R01NS104934)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- central complex, angular integration, Drosophila, spatial navigation, persistent activity, turning behavior, neural circuit architecture, angular velocity
- MeSH terms
- Animals, Darkness, Drosophila melanogaster, Female, Flight, Animal, Models, Neurological, Neural Pathways, Neurons, Orientation, Rotation, Space Perception, Walking, Spatio-Temporal Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
