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Cited by 50Neurobiology and Insect Physiology ResearchMotor Control and AdaptationMultisensory perception and integration

Spatial Comparisons of Mechanosensory Information Govern the Grooming Sequence in Drosophila

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Zhang, Neil, Guo, Li, Simpson, Julie H.·2020·Current Biology
DOI 10.1016/j.cub.2020.01.045PMC PMC7184881
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Abstract

Animals integrate information from different sensory modalities, body parts, and time points to inform behavioral choice, but the relevant sensory comparisons and the underlying neural circuits are still largely unknown. We use the grooming behavior of Drosophila melanogaster as a model to investigate the sensory comparisons that govern a motor sequence. Flies perform grooming movements spontaneously, but when covered with dust, they clean their bodies following an anterior-to-posterior sequence. After investigating different sensory modalities that could detect dust, we focus on mechanosensory bristle neurons, whose optogenetic activation induces a similar sequence. Computational modeling predicts that higher sensory input strength to the head will cause anterior grooming to occur first. We test this prediction using an optogenetic competition assay whereby two targeted light beams independently activate mechanosensory bristle neurons on different body parts. We find that the initial choice of grooming movement is determined by the ratio of sensory inputs to different body parts. In dust-covered flies, sensory inputs change as a result of successful cleaning movements. Simulations from our model suggest that this change results in sequence progression. One possibility is that flies perform frequent comparisons between anterior and posterior sensory inputs, and the changing ratios drive different behavior choices. Alternatively, flies may track the temporal change in sensory input to a given body part to measure cleaning effectiveness. The first hypothesis is supported by our optogenetic competition experiments: iterative spatial comparisons of sensory inputs between body parts is essential for organizing grooming movements in sequence.

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  • Computational activation of mechanosensory neurons predicts activation of a small set of neurons comprising the antennal grooming circuit, and accurately describes the circuit response upon activation of different mechanosensory subtypes.

    “Additionally, we applied this model to mechanosensory circuits and found that computational activation of mechanosensory neurons predicts activation of a small set of neurons comprising the antennal grooming circuit, and accurately describes the circuit response upon activation of different mechanosensory subtypes6–10.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [10]

    The Results sections on modeling and mechanosensory subtypes report that a model predicts grooming-action choices from sensory inputs and that activating different mechanosensory subtypes produces different grooming behaviors (page numbers unavailable). They do not report computationally predicted activation of a small set of antennal-grooming-circuit neurons or an accurate prediction of that circuit’s responses. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • The antennal grooming circuit has well-defined sensory inputs and a discrete, easily quantified behavioural output: antennal grooming behaviour.

    “As with the feeding initiation circuit, the antennal grooming circuit has well-defined sensory inputs, and a discrete, easily quantified behavioural output: antennal grooming behaviour.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [10]

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Research works printed but not linked: 43

  1. [1]Clowney EJ, Iguchi S, Bussell JJ, Scheer E, and Ruta V (2015). Multimodal Chemosensory Circuits Controlling Male Courtship in Drosophila. Neuron 87, 1036– 1049. 26279475 PMC4560615
  2. [2]Gepner R, Mihovilovic Skanata M, Bernat NM, Kaplow M, and Gershow M (2015). Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration. eLife 4, 10.7554. PMC4466338 25945916
  3. [3]Kaas JH, Nelson RJ, Sur M, Lin CS, and Merzenich MM (1979). Multiple representations of the body within the primary somatosensory cortex of primates. Science 204, 521– 523. 107591
  4. [4]Tsubouchi A, Yano T, Yokoyama TK, Murtin C, Otsuna H, and Ito K (2017). Topological and modality-specific representation of somatosensory information in the fly brain. Science 358, 615– 623. 29097543
  5. [5]Liu M, Sharma AK, Shaevitz JW, and Leifer AM (2018). Temporal processing and context dependency in Caenorhabditis elegans response to mechanosensation. eLife 7, e36419. 29943731 PMC6054533
  6. [6]Pierce-Shimomura JT, Morse TM, and Lockery SR (1999). The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci 19, 9557– 9569. 10531458 PMC6782915
  7. [7]Seeds AM, Ravbar P, Chung P, Hampel S, Midgley FM Jr., Mensh BD, and Simpson JH (2014). A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila. eLife 3, e02951. 25139955 PMC4136539
  8. [8]Qiao B, Li C, Allen VW, Shirasu-Hiza M, and Syed S (2018). Automated analysis of long-term grooming behavior in Drosophila using a k-nearest neighbors classifier. eLife 7, e34497. 29485401 PMC5860874
  9. [9]McKellar CE, Lillvis JL, Bath DE, Fitzgerald JE, Cannon JG, Simpson JH, and Dickson BJ (2019). Threshold-Based Ordering of Sequential Actions during Drosophila Courtship. Curr. Biol 29, 426– 434.e6. 30661796
  10. [10]Long MA, Jin DZ, and Fee MS (2010). Support for a synaptic chain model of neuronal sequence generation. Nature 468, 394– 399. 20972420 PMC2998755
  11. [11]Kornfeld J, Benezra SE, Narayanan RT, Svara F, Egger R, Oberlaender M, Denk W, and Long MA (2017). EM connectomics reveals axonal target variation in a sequence-generating network. eLife 6, e24364. 28346140 PMC5400503
  12. [12]Geddes CE, Li H, and Jin X (2018). Optogenetic Editing Reveals the Hierarchical Organization of Learned Action Sequences. Cell 174, 32– 43.e15. 29958111 PMC6056013
  13. [13]Simpson JH, and Looger LL (2018). Functional Imaging and Optogenetics in Drosophila. Genetics 208, 1291– 1309. 29618589 PMC5887132
  14. [14]Dombeck DA, and Reiser MB (2012). Real neuroscience in virtual worlds. Curr. Opin. Neurobiol 22, 3– 10. 22138559
  15. [15]Ravbar P, Branson K, and Simpson JH (2019). An automatic behavior recognition system classifies animal behaviors using movements and their temporal context. J. Neurosci. Methods 326, 108352. 31415845 PMC6779137
  16. [17]Tuthill JC, and Wilson RI (2016). Mechanosensation and Adaptive Motor Control in Insects. Curr. Biol 26, R1022– R1038. 27780045 PMC5120761
  17. [18]Hampel S, McKellar CE, Simpson JH, and Seeds AM (2017). Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila. eLife 6, e28804. 28887878 PMC5614557
  18. [20]Corfas G, and Dudai Y (1989). Habituation and dishabituation of a cleaning reflex in normal and mutant Drosophila. J. Neurosci 9, 56– 62. 2913213 PMC6569995
  19. [21]Li J, Zhang W, Guo Z, Wu S, Jan LY, and Jan Y-N (2016). A Defensive Kicking Behavior in Response to Mechanical Stimuli Mediated by Drosophila Wing Margin Bristles. J. Neurosci 36, 11275– 11282. 27807168 PMC5148243
  20. [23]Pfeiffer BD, Ngo T-TB, Hibbard KL, Murphy C, Jenett A, Truman JW, and Rubin GM (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735– 755. 20697123 PMC2942869
  21. [24]Yorozu S, Wong A, Fischer BJ, Dankert H, Kernan MJ, Kamikouchi A, Ito K, and Anderson DJ (2009). Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458, 201– 205. 19279637 PMC2755041
  22. [26]Mamiya A, Gurung P, and Tuthill JC (2018). Neural Coding of Leg Proprioception in Drosophila. Neuron 100, 636– 650.e6. 30293823 PMC6481666
  23. [27]Dickinson MH, and Palka J (1987). Physiological properties, time of development, and central projection are correlated in the wing mechano-receptors of Drosophila. J. Neurosci 7, 4201– 4208. 3694271 PMC6569114
  24. [28]Desai BS, Chadha A, and Cook B (2014). The stum gene is essential for mechanical sensing in proprioceptive neurons. Science 343, 1256– 1259. 24626929
  25. [29]Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F, Deisseroth K, and Tracey WD (2007). Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol 17, 2105– 2116. 18060782 PMC2225350
  26. [32]Walker RG, Willingham AT, and Zuker CS (2000). A Drosophila mechanosensory transduction channel. Science 287, 2229– 2234. 10744543
  27. [33]Cadigan KM, and Nusse R (1996). Wingless signaling in the Drosophila eye and embryonic epidermis. Development 122, 2801– 2812. 8787754
  28. [34]Baines RA, Uhler JP, Thompson A, Sweeney ST, and Bate M (2001). Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci 21, 1523– 1531. 11222642 PMC6762927
  29. [36]Hodge JJL (2009). Ion channels to inactivate neurons in Drosophila. Front. Mol. Neurosci 2, 13. 19750193 PMC2741205
  30. [37]Pézier A, Jezzini SH, Marie B, and Blagburn JM (2014). Engrailed alters the specificity of synaptic connections of Drosophila auditory neurons with the giant fiber. J. Neurosci 34, 11691– 11704. 25164665 PMC4145173
  31. [38]Thum AS, Knapek S, Rister J, Dierichs-Schmitt E, Heisenberg M, and Tanimoto H (2006). Differential potencies of effector genes in adult Drosophila. J. Comp. Neurol 498, 194– 203. 16856137
  32. [39]Montell C (2009). A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol 19, 345– 353. 19660932 PMC2747619
  33. [40]Yanagawa A, Guigue AMA, and Marion-Poll F (2014). Hygienic grooming is induced by contact chemicals in Drosophila melanogaster. Front. Behav. Neurosci 8, 254. 25100963 PMC4107972
  34. [41]Stensmyr MC, Dweck HKM, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, (2012). A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345– 1357. 23217715
  35. [42]Böröczky K, Wada-Katsumata A, Batchelor D, Zhukovskaya M, and Schal C (2013). Insects groom their antennae to enhance olfactory acuity. Proc. Natl. Acad. Sci. USA 110, 3615– 3620. 23382193 PMC3587213
  36. [43]Montell C (2012). Drosophila visual transduction. Trends Neurosci. 35, 356– 363. 22498302 PMC3367115
  37. [44]Cadigan KM, Jou AD, and Nusse R (2002). Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of Daughterless. Development 129, 3393– 3402. 12091309
  38. [45]Roseland CR, and Schneiderman HA (1979). Regulation and metamorphosis of the abdominal histoblasts ofDrosophila melanogaster. Wilehm Roux Arch. Dev. Biol 186, 235– 265. 28304946
  39. [46]Hartenstein V, and Posakony JW (1989). Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107, 389– 405. 2517255
  40. [48]Suver MP, Matheson AMM, Sarkar S, Damiata M, Schoppik D, and Nagel KI (2019). Encoding of Wind Direction by Central Neurons in Drosophila. Neuron 102, 828– 842.e7. 30948249 PMC6533146
  41. [49]Luo J, Shen WL, and Montell C (2017). TRPA1 mediates sensation of the rate of temperature change in Drosophila larvae. Nat. Neurosci 20, 34– 41. 27749829 PMC5191986
  42. [50]Tuthill JC, and Wilson RI (2016). Parallel Transformation of Tactile Signals in Central Circuits of Drosophila. Cell 164, 1046– 1059. 26919434 PMC4879191
  43. [51]von Reyn CR, Breads P, Peek MY, Zheng GZ, Williamson WR, Lee AL, Leonardo A, and Card GM (2014). A spike-timing mechanism for action selection. Nat Neurosci 17, 962– 970. 24908103

Cited by

Sorted by citations

Authors
Zhang, N., Guo, L., & Simpson, J. H.
Affiliations
University of California, Santa Barbara (US)
Corresponding author
Simpson, Julie H.
ORCID
Venue
Current Biology
Publisher
Elsevier BV
Published
2020-03
Volume
30
Issue
6
Pages
988-1001.e4
ISSN
0960-9822 (ISSN-L)
DOI
10.1016/j.cub.2020.01.045
PMC
PMC7184881
OpenAlex
W3000366174
Cited by
50
References
7
Citations by year
2026: 9 · 2025: 9 · 2024: 11 · 2023: 9 · 2022: 5 · 2021: 4 · 2020: 3
FWCI
2.41
Type
journal article
Language
en
Update notices
erratum (2020-09-21)
Open access
Licence
Locations
  • Current Biology (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
National Institutes of Health
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Keywords
grooming, Drosophila melanogaster, sensory integration, dust detection, computational modeling of behavior, behavioral choice, cleaning effectiveness
MeSH terms
Animals, Drosophila melanogaster, Grooming, Male, Neurons, Mechanotransduction, Cellular, Optogenetics

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