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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]
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]
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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
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)
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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
Chaudhuri, R., Gerçek, B., Pandey, B., Peyrache, A., & Fiete, I. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0460-x · Cited by 388
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Angular velocity integration in a fly heading circuit
Turner-Evans, D., Wegener, S., Rouault, H., Franconville, R., Wolff, T., Seelig, J. D., Druckmann, S., & Jayaraman, V. (2017) · eLife · doi:10.7554/elife.23496 · Cited by 281
“…another possibility that could explain the bump’s movements is raised by a parallel study, which provides further evidence for P-ENs serving a role in angular inte- gration and describes a second subtype of P-EN neurons that likely also influences the position of the E-PG bump (Green et al., 2017).”
ResultAttractor and integrator networks in the brain
Khona, M., & Fiete, I. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00642-0 · Cited by 356
“In a striking example of convergent evolution [155, 151], Drosophila compute HD estimates using apparently very similar dynamics [156, 157, 153, 152].”
MethodThe insect central complex and the neural basis of navigational strategies
Honkanen, A., Adden, A., da Silva Freitas, J., & Heinze, S. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.188854 · Cited by 238
“In flies, visual landmarks (Seelig and Jayaraman, 2013), rotational optic flow and non-visual angular velocity cues (Green et al., 2017; Turner-Evans et al., 2017) were shown to mediate direction coding in neurons homologous to the sky compass neurons.”
BackgroundDistinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning
Handler, A., Graham, T. G. W., Cohn, R., Morantte, I. G., Siliciano, A. F., Zeng, J., Li, Y., & Ruta, V. (2019) · Cell · doi:10.1016/j.cell.2019.05.040 · Cited by 231
Building an allocentric travelling direction signal via vector computation
Lyu, C., Abbott, L. F., & Maimon, G. (2022) · Nature · doi:10.1038/s41586-021-04067-0 · Cited by 215
Self-citationPrinciples of insect path integration
Heinze, S., Narendra, A., & Cheung, A. (2018) · Current Biology · doi:10.1016/j.cub.2018.04.058 · Cited by 195
“The second input pathway is less well described, but, in contrast, its effects on the circuit have been clearly revealed [94,95,104].”
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“…amounts of sensory data from different modalities fan into the ellipsoid body, which uses these data to construct representations of visual space and the animal’s position and orientation within it (Green et al., 2017; Heinze and Homberg, 2007; Kim et al., 2017; Seelig and Jayaraman, 2015, 2013).”
MethodA unifying perspective on neural manifolds and circuits for cognition
Langdon, C., Genkin, M., & Engel, T. A. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00693-x · Cited by 226
Generation of stable heading representations in diverse visual scenes
Kim, S. S., Hermundstad, A. M., Romani, S., Abbott, L. F., & Jayaraman, V. (2019) · Nature · doi:10.1038/s41586-019-1767-1 · Cited by 172
Sensorimotor experience remaps visual input to a heading-direction network
Fisher, Y. E., Lu, J., D’Alessandro, I., & Wilson, R. I. (2019) · Nature · doi:10.1038/s41586-019-1772-4 · Cited by 165
Wolff, T., & Rubin, G. M. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24512 · Cited by 156
“The central complex has been suggested to contain a ring attractor network (Kim, Rouault, Druckmann, & Jayaraman, 2017; Seelig & Jayaraman, 2015) that maintains a representation of the fly's heading direction that may be useful for navigation and orientation in visual conditions as well as in darkness (Green et al., 2…”
BackgroundSun Navigation Requires Compass Neurons in Drosophila
Giraldo, Y. M., Leitch, K. J., Ros, I. G., Warren, T. L., Weir, P. T., & Dickinson, M. H. (2018) · Current Biology · doi:10.1016/j.cub.2018.07.002 · Cited by 161
The Neuroanatomical Ultrastructure and Function of a Biological Ring Attractor
Turner-Evans, D. B., Jensen, K. T., Ali, S., Paterson, T., Sheridan, A., Ray, R. P., Wolff, T., Lauritzen, J. S., Rubin, G. M., Bock, D. D., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.006 · Cited by 168
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Feinerman, O., Pinkoviezky, I., Gelblum, A., Fonio, E., & Gov, N. S. (2018) · Nature Physics · doi:10.1038/s41567-018-0107-y · Cited by 175
The neuroanatomical ultrastructure and function of a biological ring attractor
Turner-Evans, D. B., Jensen, K. T., Ali, S., Paterson, T., Sheridan, A., Ray, R. P., Wolff, T., Lauritzen, S., Rubin, G. M., Bock, D., et al. (2019) · doi:10.1101/847152 · Cited by 166
“In a recent study, Green et al. reported that E-PG and P-EN2 activity in the PB are anticorrelated (Green et al., 2017), which we also observe (data not shown).”
InfluentialTransforming representations of movement from body- to world-centric space
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“EB projection neurons (EPG neurons or “compass neurons”) send this heading information to the protocerebral bridge (PB) 7,8 (Fig.”
Self-citationMechanisms Underlying the Neural Computation of Head Direction
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“For example, the two PEN neurons below have very similar morphology but quite distinct inputs, as shown in Fig 7 (PEN1 and PEN2 neurons, in fact, have been shown to have different functional activity in [34]).”
BackgroundSexual arousal gates visual processing during Drosophila courtship
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Self-citationA Neural Network for Wind-Guided Compass Navigation
Okubo, T. S., Patella, P., D’Alessandro, I., & Wilson, R. I. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.022 · Cited by 114
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BackgroundMethodInfluentialNetwork statistics of the whole-brain connectome of Drosophila
Lin, A., Yang, R., Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Costa, M., Eichler, K., et al. (2024) · Nature · doi:10.1038/s41586-024-07968-y · Cited by 147
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Unraveling the neural basis of insect navigation
Heinze, S. (2017) · Current Opinion in Insect Science · doi:10.1016/j.cois.2017.09.001 · Cited by 132
“[PubMed: 28530551] [** Together with [28] this paper reveals that recurrent connections between ‘wedge’ and ‘tile’ neurons of the fly central complex form the basis for integrating rotational movements of the fly into an updated head-direction signal.”
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Bidaye, S. S., Laturney, M., Chang, A. K., Liu, Y., Bockemühl, T., Büschges, A., & Scott, K. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.032 · Cited by 109
A visual pathway for skylight polarization processing in Drosophila
Hardcastle, B. J., Omoto, J. J., Kandimalla, P., Nguyen, B.-C. M., Keleş, M. F., Boyd, N. K., Hartenstein, V., & Frye, M. A. (2021) · eLife · doi:10.7554/elife.63225 · Cited by 111
Building a functional connectome of the Drosophila central complex
Franconville, R., Beron, C. C., & Jayaraman, V. (2018) · eLife · doi:10.7554/elife.37017 · Cited by 129
“‘New Type Name’ refers to the nomenclature for short names adopted in this paper (following [Kakaria and de Bivort, 2017; Turner-Evans et al., 2017; Green et al., 2017]).”
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Functional Imaging and Optogenetics in Drosophila
Simpson, J. H., & Looger, L. L. (2018) · Genetics · doi:10.1534/genetics.117.300228 · Cited by 119
“…(Kim et al. 2017; Turner-Evans et al. 2017) elucidated how a circuit in 1300 J. H. Simpson and L. L. Looger the adult fly’s central complex uses angular velocity integration to update a representation of head direction [a mechanism independently identified in a parallel study (Green et al. 2017)].”
BackgroundMethodConverting an allocentric goal into an egocentric steering signal
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“For both two-photon calcium imaging and patch-clamp experiments, we placed flies in a virtual reality setup described previously 34 .”
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Sun, X., Yue, S., & Mangan, M. (2020) · eLife · doi:10.7554/elife.54026 · Cited by 96
“Insects track their orientation through head-direction cells Seelig and Jayaraman, 2015 whose concurrent firing pattern forms a single bump of activity that shifts around the ring as the animal turns (measured through local visual [Green et al., 2017; Turner-Evans et al., 2017], global visual (Heinze and Homberg, 2007…”
The head direction circuit of two insect species
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Decoding locomotion from population neural activity in moving C. elegans
Hallinen, K. M., Dempsey, R., Scholz, M., Yu, X., Linder, A. N., Randi, F., Sharma, A. K., Shaevitz, J. W., & Leifer, A. M. (2021) · eLife · doi:10.7554/elife.66135 · Cited by 112
“For example, population recordings from the central complex in Drosophila reveal that the animal’s heading is represented in the population by a bump of neural activity in a ring attractor network (Kim et al., 2017; Green et al., 2017).”
Savelli, F., & Knierim, J. J. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.188912 · Cited by 93
“Vice versa, a process conceptually and computationally equivalent to path integration can be applied to a purely directional reference frame – based on the integration of angular velocity to update orientation irrespective of position – as occurs in the nervous system (Green et al., 2017; Knierim and Zhang, 2012; Skag…”
BackgroundMultisensory coding of angular head velocity in the retrosplenial cortex
Keshavarzi, S., Bracey, E. F., Faville, R., Campagner, D., Tyson, A. L., Lenzi, S. C., Branco, T., & Margrie, T. W. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.031 · Cited by 94
“It is widely accepted that the updating of this heading direction signal arises from angular velocity integration (Blair and Sharp, 1995; Green et al., 2017; Laurens and Angelaki, 2018; McNaughton et al., 1991; McNaughton et al., 1995; TurnerEvans et al., 2017), with theoretical models of head direction computation re…”
BackgroundToroidal topology of population activity in grid cellsPreprint
Gardner, R. J., Hermansen, E., Pachitariu, M., Burak, Y., Baas, N. A., Dunn, B. A., Moser, M., & Moser, E. I. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.25.432776 · Cited by 91
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“Available data indicate that there are two complete linearized topographic maps of head direction in Δ7 cells, positioned side-by-side and formatted as two cycles of a sinusoidal function over neural space 5,24,47,56 .”
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Self-citationFlexible navigational computations in the Drosophila central complex
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Rayshubskiy, A., Holtz, S. L., Bates, A. S., Vanderbeck, Q. X., Capdevila, L. S., Rockwell, V., & Wilson, R. I. (2020) · doi:10.1101/2020.04.04.024703 · Cited by 64
“As expected from previous work, 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).”
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Self-citationFlight-Induced Compass Representation in the Monarch Butterfly Heading Network
Beetz, M. J., Kraus, C., 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 76
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Corfas, R. A., Sharma, T., & Dickinson, M. H. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.004 · Cited by 60
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
“35 ) or PEN1 (ref.”
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Werkhoven, Z., Bravin, A., Skutt-Kakaria, K., Reimers, P., Pallares, L. F., Ayroles, J. F., & de Bivort, B. L. (2021) · eLife · doi:10.7554/elife.64988 · Cited by 77
“…changes when we inactivated or activated neurons in the Central Complex, a cluster of neuropils involved in locomotor behaviors (Buchanan et al., 2015; Ofstad et al., 2011; Kottler et al., 2019) and heading estimation (Seelig and Nature, 2015; and Shah et al., 2017; Kakaria and de Bivort, 2017).”
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Currier, T. A., Pang, M. M., & Clandinin, T. R. (2023) · GENETICS · doi:10.1093/genetics/iyad064 · Cited by 63
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Singh, S. H., van Breugel, F., Rao, R. P. N., & Brunton, B. W. (2023) · Nature Machine Intelligence · doi:10.1038/s42256-022-00599-w · Cited by 61
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el Jundi, B., Warrant, E. J., Pfeiffer, K., & Dacke, M. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24520 · Cited by 67
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Currier, T. A., Matheson, A. M. M., & Nagel, K. I. (2020) · eLife · doi:10.7554/elife.61510 · Cited by 60
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Shiozaki, H. M., & Kazama, H. (2017) · Nature Neuroscience · doi:10.1038/nn.4628 · Cited by 65
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“…publications have provided some substantial experimental evidence towards an additional integration of orientation angles and angular velocity: Green et al. (2017) and Turner-Evans et al. (2017) have identified a type of neuron (tile neuron) which connects the EB to the PB. Activity in these…”
BackgroundA DNAzyme-powered cross-catalytic circuit for amplified intracellular imaging
Zou, L., Wu, Q. D., Zhou, Y., Gong, X. Q., Liu, X., & Wang, F. (2019) · Chemical Communications · doi:10.1039/c9cc02637a · Cited by 60
Brain-wide representations of ongoing behavior: a universal principle?
Kaplan, H. S., & Zimmer, M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.02.008 · Cited by 59
A brainstem integrator for self-location memory and positional homeostasis in zebrafish
Yang, E., Zwart, M., James, B., Rubinov, M., Wei, Z., Narayan, S., Vladimirov, N., Mensh, B. D., Fitzgerald, J. E., & Ahrens, M. B. (2022) · Cell · doi:10.1016/j.cell.2022.11.022 · Cited by 63
Mapping the neural dynamics of locomotion across the Drosophila brain
Brezovec, B. E., Berger, A. B., Hao, Y. A., Chen, F., Druckmann, S., & Clandinin, T. R. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.063 · Cited by 58
Functional network topography of the medial entorhinal cortex
Obenhaus, H. A., Zong, W., Jacobsen, R. I., Rose, T., Donato, F., Chen, L., Cheng, H., Bonhoeffer, T., Moser, M., & Moser, E. I. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2121655119 · Cited by 57
“One of the best illustrations of this concept in non-mammalian species is the discovery of a ring-shaped head-direction (HD) circuit in the centroid complex of fruit flies (Green et al., 2017; Kim et al., 2017; Seelig and Jayaraman, 2015), whose anatomical layout and wiring mirrors the predictions of ring attractor ne…”
BackgroundSchilling, M., & Cruse, H. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007804 · Cited by 56
Connectomics and the neural basis of behaviour
Galili, D. S., Jefferis, G. S. X. E., & Costa, M. (2022) · Current Opinion in Insect Science · doi:10.1016/j.cois.2022.100968 · Cited by 55
“This circuit relies on combining both internal self-motion cues (angular velocity) [55,56] and external cues (polarised light, visual landmarks, mechanosensory wind cues or others), carried by ring neurons.”
BackgroundHulse, 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
“Within the PB, FB columnar neurons inherit a head direction bump directly from EPG neurons and indirectly through Δ7 neurons (Figure 68Bi) (Franconville et al., 2018; Green et al., 2017; Turner-Evans et al., 2017; Turner-Evans et al., 2020).”
BackgroundResultInfluentialZittrell, F., Pfeiffer, K., & Homberg, U. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2005192117 · Cited by 52
“heading signals are represented in the CX in a compass-like, topographic fashion (4, 8, 16, 28, 29).”
BackgroundInfluentialA Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila
Shiozaki, H., Ohta, K., & Kazama, H. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.009 · Cited by 50
Karagyozov, D., Skanata, M. M., Lesar, A., & Gershow, M. H. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.013 · Cited by 51
Gkanias, E., Risse, B., Mangan, M., & Webb, B. H. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007123 · Cited by 49
“5 ̊ degrees apart [33], whereas the fly’s compass covers at least 270 ̊, changing by around� 35 ̊ per column [34] and might be assumed to form a 360 ̊ representation of space [32].”
BackgroundFiring patterns in a fractional-order FithzHugh–Nagumo neuron model
Yao, Z., Sun, K., & He, S. (2022) · Nonlinear Dynamics · doi:10.1007/s11071-022-07690-2 · Cited by 48
The brain behind straight-line orientation in dung beetles
el Jundi, B., Baird, E., Byrne, M. J., & Dacke, M. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.192450 · Cited by 52
“Feature detection and orientation tuning in the Drosophila central complex.”
BackgroundInfluentialKottler, B., Faville, R., Bridi, J. C., & Hirth, F. (2019) · Current Biology · doi:10.1016/j.cub.2019.01.017 · Cited by 48
“, using the same Gal4 driver line, revealed that a turn is performed when the activity of a single PB glomerulus takes over the rest of the population, leading to locally restricted neuronal activity [19, 44].”
InfluentialA 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
Xie, X., Tabuchi, M., Brown, M. P., Mitchell, S. P., Wu, M. N., & Kolodkin, A. L. (2017) · eLife · doi:10.7554/elife.25328 · Cited by 46
“DOI: 10.7554/eLife.25328 2 of 33 fly’s head direction coordinates (Seelig and Jayaraman, 2015; Turner-Evans et al., 2017; Green et al., 2017).”
BackgroundInfluentialSullivan, L. F., Warren, T. L., & Doe, C. Q. (2019) · eLife · doi:10.7554/elife.43482 · Cited by 46
Madhav, M. S., & Cowan, N. J. (2020) · Annual Review of Control Robotics and Autonomous Systems · doi:10.1146/annurev-control-060117-104856 · Cited by 49
“An apparatus that allows two-photon calcium imaging while head-fixed flies walk on an air-supported ball (145) enabled the discovery of a neural correlate of the hypothesized ring-attractor angular integration system for encoding orientation in the central complex of flies (146, 147).”
BackgroundConnectomic 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 45
“1a), where they together form a complex recurrent neural network 5,41,42 (Fig.”
Self-Organized Attractor Dynamics in the Developing Head Direction Circuit
Bassett, J. P., Wills, T. J., & Cacucci, F. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.010 · Cited by 41
Automated real-time quantification of group locomotor activity in Drosophila melanogaster
Scaplen, K. M., Mei, N. J., Bounds, H. A., Song, S. L., Azanchi, R., & Kaun, K. R. (2019) · Scientific Reports · doi:10.1038/s41598-019-40952-5 · Cited by 46
The brain of a nocturnal migratory insect, the Australian Bogong moth
Adden, A. K., Wibrand, S., Pfeiffer, K., Warrant, E. J., & Heinze, S. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24866 · Cited by 44
Dana, H., Sun, Y., Mohar, B., Hulse, B. K., Hasseman, J. P., Tsegaye, G., Tsang, A., Wong, A. M., Patel, R. H., Macklin, J. J., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/434589 · Cited by 44
Olfactory navigation in arthropods
Steele, T., Lanz, A. J., & Nagel, K. I. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-022-01611-9 · Cited by 45
Vision for navigation: What can we learn from ants?
Graham, P., & Philippides, A. O. (2017) · Arthropod Structure & Development · doi:10.1016/j.asd.2017.07.001 · Cited by 40
Collett, T. S. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.205187 · Cited by 43
The neuronal building blocks of the navigational toolkit in the central complex of insects
Pfeiffer, K. (2022) · Current Opinion in Insect Science · doi:10.1016/j.cois.2022.100972 · Cited by 52
Angelaki, D. E., & Laurens, J. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.12.002 · Cited by 51
Two Compasses in the Central Complex of the Locust Brain
Pegel, U., Pfeiffer, K., Zittrell, F., Scholtyssek, C., & Homberg, U. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0940-18.2019 · Cited by 42
“This range is close to the twofold representation of 360° space of E-PG neurons (equivalents to locust CL1 neurons) in the fly (Green et al., 2017), which was also a necessary assumption for a computational model of path integration in bees (Stone et al.”
BackgroundInfluentialQuantifying behavior to solve sensorimotor transformations: advances from worms and flies
Calhoun, A. J., & Murthy, M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.08.006 · Cited by 42
“Employing such a setup has already revealed many of the sensorimotor processes that underlie spatial navigation in Drosophila [63,64].”
BackgroundRecent Advances in the Genetic Dissection of Neural Circuits in Drosophila
Guo, C., Pan, Y., & Gong, Z. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-019-00390-9 · Cited by 40
Harootonian, S. K., Wilson, R. C., Hejtmánek, L., Ziskin, E. M., & Ekstrom, A. D. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007489 · Cited by 44
The cognitive (lateral) hypothalamus
Sharpe, M. J. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.08.019 · Cited by 42
One-shot entorhinal maps enable flexible navigation in novel environments
Wen, J. H., Sorscher, B., Jones, E. A. A., Ganguli, S., & Giocomo, L. M. (2024) · Nature · doi:10.1038/s41586-024-08034-3 · Cited by 49
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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