Cited by 70Neurobiology and Insect Physiology ResearchMotor Control and AdaptationNeuroscience and Neuropharmacology Research

Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila

Open access
Hampel, Stefanie, McKellar, Claire E, Simpson, Julie H, Seeds, Andrew M·2017·eLife

Published version of a preprint

Abstract

A central model that describes how behavioral sequences are produced features a neural architecture that readies different movements simultaneously, and a mechanism where prioritized suppression between the movements determines their sequential performance. We previously described a model whereby suppression drives a Drosophila grooming sequence that is induced by simultaneous activation of different sensory pathways that each elicit a distinct movement (Seeds et al., 2014). Here, we confirm this model using transgenic expression to identify and optogenetically activate sensory neurons that elicit specific grooming movements. Simultaneous activation of different sensory pathways elicits a grooming sequence that resembles the naturally induced sequence. Moreover, the sequence proceeds after the sensory excitation is terminated, indicating that a persistent trace of this excitation induces the next grooming movement once the previous one is performed. This reveals a mechanism whereby parallel sensory inputs can be integrated and stored to elicit a delayed and sequential grooming response.

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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 [9]

    The Results section, “Identification of mechanosensory neurons that elicit specific grooming movements” (page unavailable), reports that activating identified mechanosensory neurons elicits eye or wing grooming. The paper does not report computational activation predicting a small set of antennal-grooming circuit neurons or accurately describing responses to different mechanosensory subtypes; the citing sentence presents those as its authors’ own findings. (LLM, conf=0.83)

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  • 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.”

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Research works printed but not linked: 41

  1. Blagburn JM Sattelle DB 1987 Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach, Periplaneta Americana Journal of Experimental Biology 127 135 157
  2. Bullock D 2004 Adaptive neural models of queuing and timing in fluent action Trends in Cognitive Sciences 8 426 433 10.1016/j.tics.2004.07.003 15350244 · DOI
  3. Burrows M Matheson T 1994 A presynaptic gain control mechanism among sensory neurons of a locust leg proprioceptor The Journal of Neuroscience 14 272 282 8283235 PMC6576869
  4. Cadigan KM Jou AD Nusse R 2002 Wingless blocks bristle formation and morphogenetic furrow progression in the eye through repression of daughterless Development 129 3393 3402 12091309
  5. Clarac F Cattaert D 1996 Invertebrate presynaptic inhibition and motor control Experimental Brain Research 112 163 180 10.1007/BF00227635 8951385 · DOI
  6. Cole ES Palka J 1982 The pattern of campaniform sensilla on the wing and haltere of Drosophila Melanogaster and several of its homeotic mutants Journal of Embryology and Experimental Morphology 71 41 61 6818316
  7. Corfas G Dudai Y 1989 Habituation and dishabituation of a cleaning reflex in normal and mutant Drosophila The Journal of Neuroscience 9 56 62 2913213 PMC6569995
  8. Dickinson MH Palka J 1987 Physiological properties, time of development, and central projection are correlated in the wing mechanoreceptors of Drosophila The Journal of Neuroscience 7 4201 4208 3694271 PMC6569114
  9. Davis WJ 1979 Behavioural hierarchies Trends in Neurosciences 2 5 7 10.1016/0166-2236(79)90003-1 · DOI
  10. Gaudry Q Kristan WB 2009 Behavioral choice by presynaptic inhibition of tactile sensory terminals Nature Neuroscience 12 1450 1457 10.1038/nn.2400 19801989 · DOI
  11. Ghysen A 1980 The projection of sensory neurons in the central nervous system of Drosophila: Choice of the appropriate pathway Developmental Biology 78 521 541 10.1016/0012-1606(80)90351-6 7409313 · DOI
  12. Guzulaitis R Alaburda A Hounsgaard J 2013 Increased activity of pre-motor network does not change the excitability of motoneurons during protracted scratch initiation The Journal of Physiology 591 1851 1858 10.1113/jphysiol.2012.246025 23339173 PMC3624855 · DOI
  13. Hamada FN Rosenzweig M Kang K Pulver SR Ghezzi A Jegla TJ Garrity PA 2008 An internal thermal sensor controlling temperature preference in Drosophila Nature 454 217 220 10.1038/nature07001 18548007 PMC2730888 · DOI
  14. Hampel S Chung P McKellar CE Hall D Looger LL Simpson JH 2011 Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns Nature Methods 8 253 259 10.1038/nmeth.1566 21297621 PMC3077945 · DOI
  15. Hartenstein V Posakony JW 1989 Development of Adult Sensilla on the Wing and Notum of Drosophila Melanogaster Development 107 389 405 2517255
  16. Honegger HW 1977 Interommatidial hair receptor axons extending into the ventral nerve cord in the cricket Gryllus campestris Cell and Tissue Research 182 281 285 10.1007/BF00220597 902309 · DOI
  17. Honegger H-W Reif H Müller W 1979 Sensory mechanisms of eye cleaning behavior in the cricketGryllus campestris Journal of Comparative Physiology 129 247 256 10.1007/BF00657661 · DOI
  18. Hwang RY Zhong L Xu Y Johnson T Zhang F Deisseroth K Tracey WD Daniel Tracey W 2007 Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps Current Biology 17 2105 2116 10.1016/j.cub.2007.11.029 18060782 PMC2225350 · DOI
  19. Inagaki HK Jung Y Hoopfer ED Wong AM Mishra N Lin JY Tsien RY Anderson DJ 2014 Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship Nature Methods 11 325 332 10.1038/nmeth.2765 24363022 PMC4151318 · DOI · Paper page
  20. Jovanic T Schneider-Mizell CM Shao M Masson JB Denisov G Fetter RD Mensh BD Truman JW Cardona A Zlatic M 2016 Competitive disinhibition mediates behavioral choice and sequences in Drosophila Cell 167 858 870 10.1016/j.cell.2016.09.009 27720450 · DOI
  21. Kays I Cvetkovska V Chen BE 2014 Structural and functional analysis of single neurons to correlate synaptic connectivity with grooming behavior Nature Protocols 9 1 10 10.1038/nprot.2013.157 24309972 · DOI
  22. Kristan WB 2008 Neuronal decision-making circuits Current Biology 18 R928 R932 10.1016/j.cub.2008.07.081 18957243 · DOI
  23. Kristan WB 2014 Behavioral sequencing: Competitive queuing in the Fly CNS Current Biology 24 R743 R746 10.1016/j.cub.2014.06.071 25137585 · DOI
  24. Kupfermann I Weiss KR 2001 Motor program selection in simple model systems Current Opinion in Neurobiology 11 673 677 10.1016/S0959-4388(01)00267-7 11741016 · DOI
  25. Lashley KS 1951 Lloyd AJ Cerebral Mechanisms in Behavior New York, US Wiley
  26. Luan H Peabody NC Vinson CR White BH 2006 Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression Neuron 52 425 436 10.1016/j.neuron.2006.08.028 17088209 PMC1713190 · DOI · Paper page
  27. Murphey RK Possidente DR Vandervorst P Ghysen A 1989 Compartments and the Topography of Leg Afferent Projections in Drosophila The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 9 3209 3217 2552040 PMC6569667
  28. Page KL Keri LKL Matheson TT 2004 Wing hair sensilla underlying aimed hindleg scratching of the locust Journal of Experimental Biology 207 2691 2703 10.1242/jeb.01096 15201302 · DOI
  29. Palka J Lawrence PA Hart HS Stephen Hart H 1979 Neural projection patterns from homeotic tissue of Drosophila studied in bithorax mutants and mosaics Developmental Biology 69 549 575 10.1016/0012-1606(79)90311-7 108163 · DOI
  30. Palka J Malone MA Ellison RL Wigston DJ 1986 Central projections of identified drosophila sensory neurons in relation to their time of development The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 6 1822 1830 3712012 PMC6568720
  31. Pfeiffer BD Ngo T-TB Hibbard KL Murphy C Jenett A Truman JW Rubin GM 2010 Refinement of Tools for Targeted Gene Expression in Drosophila Genetics 186 735 755 10.1534/genetics.110.119917 20697123 PMC2942869 · DOI · Paper page
  32. Phillis RW Bramlage AT Wotus C Whittaker A Gramates LS Seppala D Farahanchi F Caruccio P Murphey RK 1993 Isolation of Mutations Affecting Neural Circuitry Required for Grooming Behavior in Drosophila Melanogaster Genetics 133 581 592 8454205 PMC1205345
  33. Preibisch S Saalfeld S Tomancak P 2009 Globally optimal stitching of tiled 3D microscopic image acquisitions Bioinformatics 25 1463 1465 10.1093/bioinformatics/btp184 19346324 PMC2682522 · DOI · Paper page
  34. Redgrave P Prescott TJ Gurney K 1999 The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89 1009 1023 10.1016/S0306-4522(98)00319-4 10362291 · DOI · Paper page
  35. Rudomin P Schmidt RF 1999 Presynaptic inhibition in the vertebrate spinal cord revisited Experimental Brain Research 129 1 37 10.1007/s002210050933 10550500 · DOI
  36. Seeds AM Ravbar P Chung P Hampel S Midgley FM Mensh BD Simpson JH 2014 A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila eLife 3 e02951 10.7554/eLife.02951 25139955 PMC4136539 · DOI · Paper page
  37. Smith SA Shepherd D 1996 Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique The Journal of Comparative Neurology 364 311 323 10.1002/(SICI)1096-9861(19960108)364:2<311::AID-CNE9>3.0.CO;2-8 8788252 · DOI
  38. Stein PSG 2005 Neuronal control of turtle hindlimb motor rhythms Journal of Comparative Physiology A 191 213 229 10.1007/s00359-004-0568-6 15452660 · DOI
  39. Tuthill JC Wilson RI 2016 Mechanosensation and adaptive motor control in insects Current Biology 26 R1022 R1038 10.1016/j.cub.2016.06.070 27780045 PMC5120761 · DOI · Paper page
  40. Yanagawa A Guigue AM Marion-Poll F 2014 Hygienic grooming is induced by contact chemicals in Drosophila melanogaster Frontiers in Behavioral Neuroscience 8 254 54 10.3389/fnbeh.2014.00254 25100963 PMC4107972 · DOI
  41. Zack S Bacon J 1981 Interommatidial sensilla of the praying mantis: Their central neural projections and role in head-cleaning behavior Journal of Neurobiology 12 55 65 10.1002/neu.480120105 7193711 · DOI

Cited by

Sorted by citations

Authors
Hampel, S., McKellar, C. E., Simpson, J. H., & Seeds, A. M.
Affiliations
Howard Hughes Medical Institute (US)
Venue
eLife
Published
2017-09-09
Volume
6
ISSN
2050-084X (ISSN-L)
OpenAlex
W2614463946
Cited by
70
References
4
Citations by year
2026: 8 · 2025: 11 · 2024: 12 · 2023: 11 · 2022: 4 · 2021: 5 · 2020: 15 · 2019: 2 · 2018: 2
FWCI
2.54
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health (GM103642, MD007600)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
grooming, behavioral sequences, parallel sensory pathways, movement suppression, sensory integration, Drosophila, optogenetic stimulation, transgene expression
MeSH terms
Afferent Pathways, Animals, Drosophila melanogaster, Grooming, Sensory Receptor Cells, Animals, Genetically Modified, Optogenetics

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