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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.
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“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
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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]
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“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]
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Items 101–200 of 336
Neural networks for navigation: From connections to computations
Wilson, R. I. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-110920-032645 · Cited by 38
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“Ultimately, we used bvjj and bv? because this representation is more closely related to movement representation within the insect brain (Green et al., 2017; Heinze, 2017; Turner-Evans and Jayaraman, 2016), and because the measurement errors associated with angular speed are particularly large when flies moves slowly (…”
MethodA neural circuit architecture for rapid learning in goal-directed navigation
Dan, C., Hulse, B. K., Kappagantula, R., Jayaraman, V., & Hermundstad, A. M. (2024) · Neuron · doi:10.1016/j.neuron.2024.04.036 · Cited by 51
“118,131 Our model relies on the projection patterns of the PFL2 and PFL3 neurons, which show phase shifts of 180 (cid:1) and 90 (cid:1) respectively between their PB and FB arbors (Figures S7D and S7F; note also that PFL2 neurons project to both left and right LALs).”
MethodOn the role of the head ganglia in posture and walking in insects
Emanuel, S., Kaiser, M., Pflueger, H.-J., & Libersat, F. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00135 · Cited by 31
“These neurons (termed EB-PB-gall or E-PG neurons) were shown to be tracking the fly’s angular movements (heading) even in darkness (Seelig and Jayaraman, 2015; Green et al., 2017; Turner-Evans et al., 2017).”
BackgroundBayesian inference in ring attractor networks
Kutschireiter, A., Basnak, M. A., Wilson, R. I., & Drugowitsch, J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2210622120 · Cited by 36
Andrade, I. V., Riebli, N., Nguyen, B.-C. M., Omoto, J. J., Fetter, R. D., Cardona, A., & Hartenstein, V. (2019) · Current Biology · doi:10.1016/j.cub.2018.12.012 · Cited by 39
Kandimalla, P., Omoto, J. J., Hong, E. J., & Hartenstein, V. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01616-y · Cited by 39
Predicting modular functions and neural coding of behavior from a synaptic wiring diagram
Vishwanathan, A., Sood, A., Wu, J., Ramirez, A. D., Yang, R., Kemnitz, N., Ih, D., Turner, N., Lee, K., Tartavull, I., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01784-3 · Cited by 36
Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types
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“Polarity of CL2 neurons of the honeybee as well as the different interhemispheric wiring schemes of CL1 and CL2 neurons meet the conditions requested by the network model for angular integration (Green et al., 2017; Turner-Evans et al., 2017), that is, CL1 and CL2 neurons arborizing in the same slice”
BackgroundInfluentialHow the insect central complex could coordinate multimodal navigation
Sun, X., Yue, S., & Mangan, M. (2021) · eLife · doi:10.7554/elife.73077 · Cited by 35
Drosophila re-zero their path integrator at the center of a fictive food patch
Behbahani, A. H., Palmer, E. H., Corfas, R. A., & Dickinson, M. H. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.006 · Cited by 31
Wind gates olfaction-driven search states in free flight
Stupski, S. D., & van Breugel, F. (2024) · Current Biology · doi:10.1016/j.cub.2024.07.009 · Cited by 32
Noorman, M., Hulse, B. K., Jayaraman, V., Romani, S., & Hermundstad, A. M. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01766-5 · Cited by 34
“However, growing evidence suggests that similar computations might be performed in much smaller brains with far fewer neurons 8,30,34,35,37,45 .”
InfluentialMultisensory control of navigation in the fruit fly
Currier, T. A., & Nagel, K. I. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.11.017 · Cited by 36
“The central complex contains representations of self-motion, including heading (Seelig 2015), angular velocity (Martin 2015, Green 2017, Turner-Evans 2017), and forward velocity (Stone 2017).”
BackgroundThe sky compass network in the brain of the desert locust
Homberg, U., Hensgen, R., Jahn, S., Pegel, U., Takahashi, N., Zittrell, F., & Pfeiffer, K. (2022) · Journal of Comparative Physiology A · doi:10.1007/s00359-022-01601-x · Cited by 38
Neural circuits for goal-directed navigation across species
Basu, J., & Nagel, K. I. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.09.005 · Cited by 35
“Similarly, the fl y compass system is required for a fl y to adopt a fi xed offset orientation from the sun, but is not necessary for orienting directly to a visual landmark [123,174].”
Multi-regional circuits underlying visually guided decision-making in Drosophila
Cheong, H. S., Siwanowicz, I., & Card, G. M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.010 · Cited by 33
“The CX plays a role in orientation [7], navigation [59] and visual memory [5,26] by maintaining an internal compass that integrates visual input and the fly’s own angular motion [60,61].”
BackgroundCortical Integration of Vestibular and Visual Cues for Navigation, Visual Processing, and Perception
Keshavarzi, S., Vélez‐Fort, M., & Margrie, T. W. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-120722-100503 · Cited by 38
“At least two types of cells identified in the rodent’s brain – as well as in other animals including insects (Green et al. 2017, Seelig & Jayaraman 2015, Turner-Evans et al. 2017), fish (Vinepinsky et al. 2020), birds (Ben-Yishay et al. 2021), bats (Finkelstein et al. 2015) and primates (Baumann &…”
How the Internally Organized Direction Sense Is Used to Navigate
Park, E., Keeley, S., Savin, C., Ranck, J. B., & Fenton, A. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.019 · Cited by 36
An On-chip Spiking Neural Network for Estimation of the Head Pose of the iCub Robot
Kreiser, R., Renner, A., Leite, V. R. C., Serhan, B., Bartolozzi, C., Glover, A., & Sandamirskaya, Y. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00551 · Cited by 31
“Animals can also navigate in large environments by combining a set of “on-board” sensors, i.e., the vestibular and vision system (Burak and Fiete, 2009; Seelig and Jayaraman, 2015; Green et al., 2017; Fisher et al., 2019).”
BackgroundMethodThe neuroethology of ant navigation
Collett, T. S., Graham, P., & Heinze, S. (2025) · Current Biology · doi:10.1016/j.cub.2024.12.034 · Cited by 34
Elucidating Neuronal Mechanisms Using Intracellular Recordings during Behavior
Lee, A. K., & Brecht, M. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.03.014 · Cited by 34
Whittington, J. C. R., Dorrell, W., Behrens, T. E. J., Ganguli, S., & El-Gaby, M. (2024) · Neuron · doi:10.1016/j.neuron.2024.10.017 · Cited by 54
From Photons to Behaviors: Neural Implementations of Visual Behaviors in Drosophila
Ryu, L., Kim, S. Y., & Kim, A. J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.883640 · Cited by 31
“, 2017) and moves the heading signal, which was later confirmed by experiments (Green et al., 2017).”
BackgroundMosheiff, N., & Burak, Y. (2019) · eLife · doi:10.7554/elife.48494 · Cited by 27
“Recent discoveries in the Drosophila melanogaster central complex point to a representation of heading that is maintained by neural circuitry with close similarity to this architecture (Seelig and Jayaraman, 2015; Turner-Evans et al., 2017; Kim et al., 2017; Green et al., 2017).”
Neural circuit mechanisms for steering control in walking Drosophila
Rayshubskiy, A., Holtz, S. L., Bates, A. S., Vanderbeck, Q. X., Serratosa Capdevila, L., Rockwell, V., & Wilson, R. (2025) · eLife · doi:10.7554/elife.102230 · Cited by 27
“Once we identified DNa02 in the FAFB dataset, we annotated all the presynaptic sites (1,497) and postsynaptic sites (10,842) within the brain domain of this neuron.”
Variations on an ancient theme — the central complex across insects
Heinze, S. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101390 · Cited by 34
“They form two recurrent loops that are the foundation for head direction coding in the insect CX [13,47–50].”
Grid Cells in Cognition: Mechanisms and Function
Dong, L. L., & Fiete, I. (2024) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101323-112047 · Cited by 33
Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons
Manjila, S. B., Kuruvilla, M., Ferveur, J., Sane, S. P., & Hasan, G. (2018) · Current Biology · doi:10.1016/j.cub.2018.11.070 · Cited by 25
“For instance, the insect central complex (CC) plays an important role in integrating information about heading direction and angular orientation of flight [2] upon motion detection in the optic medulla [3], and different regions of the CC, such as the fan-shaped body (FB), process visual information during flight [4].”
Semaphorin 2b Regulates Sleep-Circuit Formation in the Drosophila Central Brain
Xie, X., Tabuchi, M., Corver, A., Duan, G. Y., Wu, M. N., & Kolodkin, A. L. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.019 · Cited by 23
“Columns are formed perpendicular to laminae in a wide range of neural systems in many organisms, from insects to vertebrates, and the columnar organization of PB and EB circuits in the CX has been implicated in regulating insect navigation behaviors (Heinze and Homberg, 2007; Heinze et al., 2009; Seelig and Jayaraman,…”
BackgroundLearning accurate path integration in ring attractor models of the head direction system
Vafidis, P., Owald, D., D’Albis, T., & Kempter, R. (2022) · eLife · doi:10.7554/elife.69841 · Cited by 29
Emergent oscillations assist obstacle negotiation during ant cooperative transportPreprint
Gelblum, A., Pinkoviezky, I., Fonio, E., Gov, N. S., & Feinerman, O. (2021) · arXiv (Cornell University) · doi:10.48550/arxiv.2107.09508 · Cited by 26
Visual route following for tiny autonomous robots
van Dijk, T., Wagter, C. D., & de Croon, G. (2024) · Science Robotics · doi:10.1126/scirobotics.adk0310 · Cited by 31
“In recent work, the mechanisms behind path integration have been traced back all the way to the neural level, where ring attractors in the central complex play an important role ( 21 – 23 ).”
BackgroundWolff, T., Eddison, M., Chen, N., Nern, A., Sundaramurthi, P., Sitaraman, D., & Rubin, G. M. (2025) · eLife · doi:10.1101/2024.10.21.619448 · Cited by 25
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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
“…for studying the integration of sensory and internal state signals with the aim of understanding how adaptive behavioral policies are generated (Seelig and Jayaraman, 2015; Kim et al., 2017; Green et al., 2017; Giraldo et al., 2018; Okubo et al., 2020; Dan et al., 2021; Matheson et al., 2022).”
Towards a common terminology for arthropod spatial orientation
Grob, R., el Jundi, B., & Fleischmann, P. N. (2021) · Ethology Ecology & Evolution · doi:10.1080/03949370.2021.1905075 · Cited by 22
“This allows the animal to keep track of its current heading orientation (Green et al. 2017; Turner-Evans et al. 2017).”
BackgroundA Neural Model for Insect Steering Applied to Olfaction and Path Integration
Adden, A. K., Stewart, T. C., Webb, B. H., & Heinze, S. (2022) · Neural Computation · doi:10.1162/neco_a_01540 · Cited by 28
Hamid, A., Gattuso, H., Caglar, A. N., Pillai, M., Steele, T., Gonzalez, A., Nagel, K., & Syed, M. H. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.020 · Cited by 24
Representation of Haltere Oscillations and Integration with Visual Inputs in the Fly Central Complex
Kathman, N. D., & Fox, J. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1707-18.2019 · Cited by 22
“Both visual (Srinivasan, 2000; Homberg et al., 2011; Green et al., 2017; Turner-Evans et al., 2017) and proprioceptive (Wehner et al.”
BackgroundTimaeus, L., Geid, L., Sancer, G., Wernet, M. F., & Hummel, T. (2020) · iScience · doi:10.1016/j.isci.2020.101590 · Cited by 23
Emergent spatial goals in an integrative model of the insect central complex
Goulard, R., Heinze, S., & Webb, B. H. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011480 · Cited by 25
Insect Flight: State of the Field and Future Directions
Treidel, L. A., Deem, K. D., Salcedo, M. K., Dickinson, M. H., Bruce, H. S., Darveau, C.-A., Dickerson, B. H., Ellers, O., Glass, J. R., Gordon, C. M., et al. (2024) · Integrative and Comparative Biology · doi:10.1093/icb/icae106 · Cited by 24
Ho, M. C. W., Tabuchi, M., Xie, X., Brown, M. P., Luu, S., Wang, S., Kolodkin, A. L., Liu, S., & Wu, M. N. (2022) · Current Biology · doi:10.1016/j.cub.2022.09.048 · Cited by 22
A neural circuit basis for context-modulation of individual locomotor behaviorPreprint
Skutt-Kakaria, K., Reimers, P., Currier, T. A., Werkhoven, Z., & de Bivort, B. L. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/797126 · Cited by 23
“Neurons of the CX, notably the E-PG cells, have been shown to encode heading, an important idiothetic feature for path integration, while walking (Green et al., 2017; Seelig and Jayaraman, 2015; Turner-Evans et al., 2017) and in flight (Giraldo et al., 2018) and appear to contribute to ring…”
BackgroundHulse, 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
Maintaining a stable head direction representation in naturalistic visual environments
Haberkern, H., Chitnis, S. S., Hubbard, P. M., Goulet, T., Hermundstad, A. M., & Jayaraman, V. (2022) · doi:10.1101/2022.05.17.492284 · Cited by 21
“…of EPG or compass neurons that each innervate individual wedges of the toroidal ellipsoid body (EB), a substructure of the CX (Fisher et al., 2019; Green et al., 2017; Kim et al., 2019; Kim et al., 2017; Seelig and Jayaraman, 2015; Turner-Evans et al., 2017; Turner-Evans et al., 2021; Wolff et…”
BackgroundTowards a multi-level understanding in insect navigation
Moël, F. L., & Wystrach, A. (2020) · Current Opinion in Insect Science · doi:10.1016/j.cois.2020.10.006 · Cited by 21
Multilevel visuomotor control of locomotion in Drosophila
Cruz, T. L., & Chiappe, M. E. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102774 · Cited by 17
Learning a Spatial Task by Trial and Error in Drosophila
Stern, U., Srivastava, H. K., Chen, H.-L., Mohammad, F., Claridge‐Chang, A., & Yang, C.-H. (2019) · Current Biology · doi:10.1016/j.cub.2019.06.045 · Cited by 22
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
Weighting of Celestial and Terrestrial Cues in the Monarch Butterfly Central Complex
Nguyen, T. A., Beetz, M. J., Merlin, C., Pfeiffer, K., & el Jundi, B. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.862279 · Cited by 20
“, 2021), TL cells (in fruit flies termed ring neurons) synapse onto a network of heading-direction cells that flexibly encode the actual flight direction of an animal based on sensory-motor information (Seelig and Jayaraman, 2015; Green et al., 2017; Turner-Evans et al., 2017; Fisher et al., 2019; Kim et al., 2019; Ok…”
BackgroundExamining Sleep Modulation by Drosophila Ellipsoid Body Neurons
Aleman, A., Omoto, J. J., Singh, P., Nguyen, B.-C. M., Kandimalla, P., Hartenstein, V., & Donlea, J. M. (2023) · eNeuro · doi:10.1523/eneuro.0281-23.2023 · Cited by 19
“…cells are positioned in a promising intersection to relay arousal state signals from sleep control neurons to circuits that encode spatial representations of the exterior world (Seelig and Jayaraman, 2013, 2015; Liu et al., 2016; Green et al., 2017; Kim et al., 2017, 2019; Donlea et al., 2018).”
BackgroundKaiser, A., Hensgen, R., Tschirner, K., Beetz, E., Wüstenberg, H., Pfaff, M., Mota, T., & Pfeiffer, K. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25339 · Cited by 21
“In Drosophila, it has been shown, that P-EN neurons and E-PG neurons are part of the internal compass network that signals head direction with respect to an external frame of reference (Green et al., 2017; Seelig & Jayaraman, 2015; Turner-Evans et al., 2017).”
BackgroundMethodDisplacement experiments provide evidence for path integration in Drosophila
Titova, A. V., Kau, B. E., Tibor, S., Mach, J., Vo‐Doan, T. T., Wittlinger, M., & Straw, A. D. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.245289 · Cited by 16
Fiore, V. G., Kottler, B., Gu, X., & Hirth, F. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00142 · Cited by 16
“This hypothesis is supported by recent studies in Drosophila (Green et al., 2017; Turner-Evans et al., 2017) and cockroaches (Martin et al., 2015; Varga and Ritzmann, 2016) and leads to testable predictions, for example that targeted layer and/or wedge-specific activity manipulations of the EB in…”
BackgroundResultInfluentialThe role of cell lineage in the development of neuronal circuitry and function
Hartenstein, V., Omoto, J. J., & Lovick, J. K. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.01.012 · Cited by 18
Cerebellar control of a unitary head direction sense
Fallahnezhad, M., Méro, J. L., Zenelaj, X., Vincent, J. D., Rochefort, C., & Rondi‐Reig, L. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2214539120 · Cited by 17
“, 1995) and potentially resembles a single, and unique internal compass (Green et al., 2017; Hulse and Jayaraman, 2020; Kim et al., 2017; Park et al., 2019).”
Mangan, M., Floreano, D., Yasui, K., Trimmer, B. A., Gravish, N., Hauert, S., Webb, B. H., Manoonpong, P., & Szczecinski, N. S. (2023) · Bioinspiration & Biomimetics · doi:10.1088/1748-3190/acc223 · Cited by 17
Constitutive and Conditional Epitope Tagging of Endogenous G-Protein–Coupled Receptors in Drosophila
Bonanno, S. L., Sanfilippo, P., Eamani, A., Sampson, M. M., Kandagedon, B., Li, K., Burns, G. D., Makar, M. E., Zipursky, S. L., & Krantz, D. E. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.2377-23.2024 · Cited by 18
Dewar, A., Wystrach, A., Philippides, A. O., & Graham, P. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005735 · Cited by 15
“Recent work has shown the presence of a ring attractor network [9, 32, 41, 42] in the ellipsoid body of the central complex which integrates both visual and proprioceptive information.”
BackgroundTransfer of Spatial Contact Information Among Limbs and the Notion of Peripersonal Space in Insects
Dürr, V., & Schilling, M. (2018) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2018.00101 · Cited by 15
“Prominent examples include the encoding of celestial direction cues in locusts (Heinze and Homberg, 2007) and of heading direction in walking fruit flies (Green et al., 2017; Turner-Evans et al., 2017).”
BackgroundWolff, T., Eddison, M., Chen, N., Nern, A., Sundaramurthi, P., Sitaraman, D., & Rubin, G. M. (2025) · eLife · doi:10.7554/elife.104764 · Cited by 17
Mechanisms of vision in the fruit fly
de Andres-Bragado, L., & Sprecher, S. G. (2019) · Current Opinion in Insect Science · doi:10.1016/j.cois.2019.06.005 · Cited by 16
“Most of the studies hint towards the importance of the central complex in spatial orientation through different mechanisms: by the use of landmark detection [38,39], or using the so-called ‘compass cells’ to calculate the position of the sun [40], or the animal’s heading, as encoded by head-direction cells [39,41,42].”
BackgroundConverting an allocentric goal into an egocentric steering signal
Pires, P. M., Abbott, L. F., & Maimon, G. (2022) · doi:10.1101/2022.11.10.516026 · Cited by 110
Self-citationNon-Hermitian quasilocalization and ring attractor neural networks
Tanaka, H., & Nelson, D. R. (2019) · Physical review. E · doi:10.1103/physreve.99.062406 · Cited by 15
Using slow frame rate imaging to extract fast receptive fields
Mano, O., Creamer, M. S., Matulis, C. A., Salazar-Gatzimas, E., Chen, J., Zavatone-Veth, J. A., & Clark, D. A. (2019) · Nature Communications · doi:10.1038/s41467-019-12974-0 · Cited by 13
“In other cases, rates have been matched after the experiment, either by downsampling the fast variable to match the infrequent neural measurements 5,8,10,11 or by inter-polating the infrequent measurements to match the high-resolution variable 12 – 17 .”
The influence of stimulus history on directional coding in the monarch butterfly brain
Beetz, M. J., & el Jundi, B. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01633-x · Cited by 14
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
Visuo-Motor Feedback Modulates Neural Activities in the Medulla of the Honeybee,Apis mellifera
Rusch, C., Alberto, D. A. S., & Riffell, J. A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1824-20.2021 · Cited by 14
“Although feedback sensitivity to visual stimuli has been well characterized (Wolf and Heisenberg, 1991; Wolf et al., 1992; Heisenberg et al., 2001; Bahl et al., 2013), the interplay between motor gain and neural processing is less clear (Wolf and Heisenberg, 1986; Fenk et al., 2014; Paulk et al.,…”
BackgroundA gravity-based three-dimensional compass in the mouse brainPreprint
Angelaki, D. E., Ng, J., Abrego, A., Cham, H., Dickman, J. D., & Laurens, J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/570382 · Cited by 14
“…(HD) cells, which encode allocentric head orientation analogous to a "neural compass" are a primordial component of the mammalian (Taube 2007; Finkelstein et al. 2015) and fly (Seelig and Jayaraman, 2015; Green et al., 2017; Turner-Evans et al., 2017; Kim et al., 2017) spatial navigation system.”
Predicting modular functions and neural coding of behavior from a synaptic wiring diagramPreprint
Vishwanathan, A., Ramirez, A. D., Wu, J., Sood, A., Yang, R., Kemnitz, N., Ih, D., Turner, N. L., Lee, K., Tartavull, I., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.28.359620 · Cited by 14
“Low dimensional dynamical attractors have been proposed to underlie a large range of computations, from storage of working memory to reduction of noise in sensory and cognitive representations (Yoon et al., 2013; Daie et al., 2015; Kim et al., 2017; Green et al., 2017).”
BackgroundJahn, S., Althaus, V., Heckmann, J., Janning, M., Seip, A., Takahashi, N., Grigoriev, C., Kolano, J., & Homberg, U. (2023) · The Journal of Comparative Neurology · doi:10.1002/cne.25535 · Cited by 15
Neuronal calcium spikes enable vector inversion in the Drosophila brain
Ishida, I. G., Sethi, S., Mohren, T. L., Haraguchi, M., Abbott, L. F., & Maimon, G. (2025) · Cell · doi:10.1016/j.cell.2025.11.040 · Cited by 11
Self-citationNOSA, an Analytical Toolbox for Multicellular Optical Electrophysiology
Oltmanns, S., Abben, F. S., Ender, A., Aimon, S., Kovacs, R., Sigrist, S. J., Storace, D. A., Geiger, J. R. P., & Raccuglia, D. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00712 · Cited by 13
“Both neural structures are considered to be integration centers for various sensory modalities (Seelig and Jayaraman, 2013; Green et al., 2017; Sun et al., 2017; Hu et al., 2018) and play important roles in locomotion (Strauss and Heisenberg, 1993) and sleep regulation (Donlea et al., 2014; Liu et…”
BackgroundNeural Circuitry for Target Selection and Action Selection in Animal Behavior
Hoke, K. L., Hebets, E. A., & Shizuka, D. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx109 · Cited by 12
“Activity in these ellipsoid body neurons corresponds to the animal’s orientation relative to its destination (Seelig and Jayaraman 2015; Green et al. 2017; Kim et al. 2017; Turner-Evans et al. 2017).”
BackgroundNeural dynamics and architecture of the heading direction circuit in a vertebrate brainPreprint
Petrucco, L., Lavian, H., Wu, Y. K., Svara, F., Štih, V., & Portugues, R. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.27.489672 · Cited by 13
Multimodal cue integration and learning in a neural representation of head direction
Basnak, M. A., Kutschireiter, A., Okubo, T. S., Chen, A., Gorelik, P., Drugowitsch, J., & Wilson, R. I. (2025) · Nature Neuroscience · doi:10.1038/s41593-024-01823-z · Cited by 13
“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.”
The Discovery of Head Direction Cells: A Personal Account
Taube, J. S. (2024) · Hippocampus · doi:10.1002/hipo.23670 · Cited by 13
“In recent years, tremendous strides have been made in studying HD-like cells in an insect model— Drosophila (Hulse and Jayaraman 2020; Green et al. 2017).”
Han, R., Huang, H.-P., Chuang, C.-L., Yen, H.-H., Kao, W.-T., Chang, H.-Y., & Lo, C. (2021) · eNeuro · doi:10.1523/eneuro.0537-20.2021 · Cited by 12
“The model successfully demonstrated the angular errors when a fly moved in darkness (Seelig and Jayaraman, 2015) and predicted the asymmetric activity in the PB during rotation (Green et al., 2017).”
BackgroundDopamine Modulation of Drosophila Ellipsoid Body Neurons, a Nod to the Mammalian Basal Ganglia
Frighetto, G., Zordan, M. A., Castiello, U., Megighian, A., & Martin, J. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.849142 · Cited by 12
“, 2020) and are characterized by an extensive recurrent networking to update the fly’s heading (Green et al., 2017; Turner-Evans et al., 2017), we stimulated the E-PG neurons (E-PG > G5A flies) using nicotine.”
BackgroundMethodTowards a unified vision on animal navigation
Menti, G. M., Meda, N., Zordan, M. A., & Megighian, A. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15881 · Cited by 11
Path Integration: Combining Optic Flow with Compass Orientation
Collett, M., & Collett, T. S. (2017) · Current Biology · doi:10.1016/j.cub.2017.09.004 · Cited by 12
A competitive disinhibitory network for robust optic flow processing in DrosophilaPreprint
Erginkaya, M., Cruz, T. L., Brotas, M., Steck, K., Nern, A., Torrão, F., Varela, N., Bock, D. D., Reiser, M. B., & Chiappe, M. E. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.06.552150 · Cited by 12
Transforming a head direction signal into a goal-oriented steering command
Westeinde, E. A., Kellogg, E., Dawson, P. M., Lu, J., Hamburg, L., Midler, B., Druckmann, S., & Wilson, R. I. (2022) · doi:10.1101/2022.11.10.516039 · Cited by 85
Circuits for self-motion estimation and walking control in Drosophila
Chiappe, M. E. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102748 · Cited by 11
Dillon, N. R., Manning, L., Hirono, K., & Doe, C. Q. (2024) · Development · doi:10.1242/dev.202504 · Cited by 11
A vector-based strategy for olfactory navigation in Drosophila
Siliciano, A. F., Minni, S., Morton, C., Dowell, C. K., Eghbali, N. B., Busch, S. E., Rhee, J. Y., Abbott, L. F., & Ruta, V. (2026) · Nature · doi:10.1038/s41586-026-10827-7 · Cited by 13
“For recordings of EPG neurons in the protocerebral bridge, phase was calculated as described previously 59 .”
Homberg, U., Hensgen, R., Rieber, E., Seyfarth, J., Kern, M., Dippel, S., Dircksen, H., Spänig, L., & Kina, Y. P. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25062 · Cited by 11
“…desert locust Schistocerca gregaria, the central complex has an internal compass-like organization with topographic 360 representations of space (Green et al., 2017; Heinze & Homberg, 2007; Pegel, Pfeiffer, Scholtyssek, & Homberg, 2019; Zittrell, Pfeiffer, & Homberg, 2020; Seelig & Jayaraman,…”
BackgroundNeural Coding: Bumps on the Move
Heinze, S. (2017) · Current Biology · doi:10.1016/j.cub.2017.03.072 · Cited by 12
Multiple head direction signals within entorhinal cortex: origin and function
Munn, R. G. K., & Giocomo, L. M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.01.015 · Cited by 12
Takahashi, N., Zittrell, F., Hensgen, R., & Homberg, U. (2022) · Journal of Experimental Biology · doi:10.1242/jeb.243858 · Cited by 11
Multiple bumps can enhance robustness to noise in continuous attractor networks
Wang, R., & Kang, L. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010547 · Cited by 10
Insect Navigation: How Flies Keep Track of Their Snack
el Jundi, B. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.051 · Cited by 9
Online learning for orientation estimation during translation in an insect ring attractor network
Robinson, B. S., Norman-Tenazas, R., Cervantes, M., Symonette, D., Johnson, E. C., Joyce, J., Rivlin, P. K., Hwang, G. M., Zhang, K., & Gray-Roncal, W. (2022) · Scientific Reports · doi:10.1038/s41598-022-05798-4 · Cited by 10
Wosnitza, A., Martin, J. P., Pollack, A. J., Svenson, G. J., & Ritzmann, R. E. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.893004 · Cited by 10
The population dynamics of a canonical cognitive circuitPreprint
Chaudhuri, R., Gerçek, B., Pandey, B., Peyrache, A., & Fiete, I. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/516021 · Cited by 10
Symmetries and Continuous Attractors in Disordered Neural CircuitsPreprint
Clark, D. G., Abbott, L. F., & Sompolinsky, H. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.26.634933 · Cited by 10
Yang, G., Wang, Y., Xu, Z., Zhang, X., Ruan, W., Mo, F., Lu, B., Fan, P., Dai, Y., He, E., et al. (2023) · Biosensors · doi:10.3390/bios13050496 · Cited by 9
“Identification of HD and Non-HD Cells Neural spikes in the RSC were recorded while the rats explored the stable environment (Control), during visual–vestibular input dissociation (Rotating), and once more when stable (Recovery) in sequence (Figure 3A).”
BackgroundInfluentialTheory of morphodynamic information processing: Linking sensing to behaviour
Juusola, M., Takalo, J., Kemppainen, J., Haghighi, K. R., Scales, B., McManus, J., Bridges, A. D., MaBouDi, H., & Chıttka, L. (2025) · Vision Research · doi:10.1016/j.visres.2024.108537 · Cited by 11
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
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