Skip to main content
SpringerLink
Log in

A Neuronal Pathway that Commands Deceleration in Drosophila Larval Light-Avoidance

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

When facing a sudden danger or aversive condition while engaged in on-going forward motion, animals transiently slow down and make a turn to escape. The neural mechanisms underlying stimulation-induced deceleration in avoidance behavior are largely unknown. Here, we report that in Drosophila larvae, light-induced deceleration was commanded by a continuous neural pathway that included prothoracicotropic hormone neurons, eclosion hormone neurons, and tyrosine decarboxylase 2 motor neurons (the PET pathway). Inhibiting neurons in the PET pathway led to defects in light-avoidance due to insufficient deceleration and head casting. On the other hand, activation of PET pathway neurons specifically caused immediate deceleration in larval locomotion. Our findings reveal a neural substrate for the emergent deceleration response and provide a new understanding of the relationship between behavioral modules in animal avoidance responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Bidaye SS, Machacek C, Wu Y, Dickson BJ. Neuronal control of Drosophila walking direction. Science 2014, 344: 97–101.

    Article  CAS  PubMed  Google Scholar 

  2. Sen R, Wu M, Branson K, Robie A, Rubin GM, Dickson BJ. Moonwalker Descending Neurons Mediate Visually Evoked Retreat in Drosophila. Curr Biol 2017, 27: 766–771.

    Article  CAS  PubMed  Google Scholar 

  3. von Reyn CR, Breads P, Peek MY, Zheng GZ, Williamson WR, Yee AL, et al. A spike-timing mechanism for action selection. Nat Neurosci 2014, 17: 962–970.

    Article  CAS  Google Scholar 

  4. von Reyn CR, Nern A, Williamson WR, Breads P, Wu M, Namiki S, et al. Feature Integration Drives Probabilistic Behavior in the Drosophila Escape Response. Neuron 2017, 94: 1190–1204 e1196.

    Google Scholar 

  5. Wu M, Nern A, Williamson WR, Morimoto MM, Reiser MB, Card GM, et al. Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs. Elife 2016, 5.

  6. Gomez-Marin A, Stephens GJ, Louis M. Active sampling and decision making in Drosophila chemotaxis. Nat Commun 2011, 2: 441.

    Article  PubMed  CAS  Google Scholar 

  7. Lahiri S, Shen K, Klein M, Tang A, Kane E, Gershow M, et al. Two alternating motor programs drive navigation in Drosophila larva. PLoS One 2011, 6: e23180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kane EA, Gershow M, Afonso B, Larderet I, Klein M, Carter AR, et al. Sensorimotor structure of Drosophila larva phototaxis. Proc Natl Acad Sci U S A 2013, 110: E3868–3877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Tastekin I, Riedl J, Schilling-Kurz V, Gomez-Marin A, Truman JW, Louis M. Role of the subesophageal zone in sensorimotor control of orientation in Drosophila larva. Curr Biol 2015, 25: 1448–1460.

    Article  CAS  PubMed  Google Scholar 

  10. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 2006, 52: 751–766.

    Article  CAS  PubMed  Google Scholar 

  11. Grillner S, Robertson B. The basal ganglia downstream control of brainstem motor centres-an evolutionarily conserved strategy. Curr Opin Neurobiol 2015, 33: 47–52.

    Article  CAS  PubMed  Google Scholar 

  12. Kiehn O. Decoding the organization of spinal circuits that control locomotion. Nat Rev Neurosci 2016, 17: 224–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ryczko D, Auclair F, Cabelguen JM, Dubuc R. The mesencephalic locomotor region sends a bilateral glutamatergic drive to hindbrain reticulospinal neurons in a tetrapod. J Comp Neurol 2016, 524: 1361–1383.

    Article  CAS  PubMed  Google Scholar 

  14. Caggiano V, Leiras R, Goni-Erro H, Masini D, Bellardita C, Bouvier J, et al. Midbrain circuits that set locomotor speed and gait selection. Nature 2018, 553: 455–460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kernan M, Cowan D, Zuker C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 1994, 12: 1195–1206.

    Article  CAS  PubMed  Google Scholar 

  16. Perrins R, Walford A, Roberts A. Sensory activation and role of inhibitory reticulospinal neurons that stop swimming in hatchling frog tadpoles. J Neurosci 2002, 22: 4229–4240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bouvier J, Caggiano V, Leiras R, Caldeira V, Bellardita C, Balueva K, et al. Descending Command Neurons in the Brainstem that Halt Locomotion. Cell 2015, 163: 1191–1203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Juvin L, Gratsch S, Trillaud-Doppia E, Gariepy JF, Buschges A, Dubuc R. A Specific Population of Reticulospinal Neurons Controls the Termination of Locomotion. Cell Rep 2016, 15: 2377–2386.

    Article  CAS  PubMed  Google Scholar 

  19. Zhao W, Gong C, Ouyang Z, Wang P, Wang J, Zhou P, et al. Turns with multiple and single head cast mediate Drosophila larval light avoidance. PLoS One 2017, 12: e0181193.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Gershow M, Berck M, Mathew D, Luo L, Kane EA, Carlson JR, et al. Controlling airborne cues to study small animal navigation. Nat Methods 2012, 9: 290–296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 2010, 468: 921–926.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mazzoni EO, Desplan C, Blau J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 2005, 45: 293–300.

    Article  CAS  PubMed  Google Scholar 

  23. Collins B, Kane EA, Reeves DC, Akabas MH, Blau J. Balance of activity between LN(v)s and glutamatergic dorsal clock neurons promotes robust circadian rhythms in Drosophila. Neuron 2012, 74: 706–718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Keene AC, Sprecher SG. Seeing the light: photobehavior in fruit fly larvae. Trends Neurosci 2012, 35: 104–110.

    Article  CAS  PubMed  Google Scholar 

  25. Gong Z, Liu J, Guo C, Zhou Y, Teng Y, Liu L. Two pairs of neurons in the central brain control Drosophila innate light preference. Science 2010, 330: 499–502.

    Article  CAS  PubMed  Google Scholar 

  26. Yamanaka N, Romero NM, Martin FA, Rewitz KF, Sun M, O’Connor MB, et al. Neuroendocrine control of Drosophila larval light preference. Science 2013, 341: 1113–1116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Selcho M, Millan C, Palacios-Munoz A, Ruf F, Ubillo L, Chen J, et al. Central and peripheral clocks are coupled by a neuropeptide pathway in Drosophila. Nat Commun 2017, 8: 15563.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. McBrayer Z, Ono H, Shimell M, Parvy JP, Beckstead RB, Warren JT, et al. Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev Cell 2007, 13: 857–871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hicheur H, Vieilledent S, Richardson MJ, Flash T, Berthoz A. Velocity and curvature in human locomotion along complex curved paths: a comparison with hand movements. Exp Brain Res 2005, 162: 145–154.

    Article  CAS  PubMed  Google Scholar 

  30. Zago M, Lacquaniti F, Gomez-Marin A. The speed-curvature power law in Drosophila larval locomotion. Biol Lett 2016, 12.

  31. McNabb SL, Baker JD, Agapite J, Steller H, Riddiford LM, Truman JW. Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 1997, 19: 813–823.

    Article  CAS  PubMed  Google Scholar 

  32. Zhang YQ, Rodesch CK, Broadie K. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 2002, 34: 142–145.

    Article  CAS  PubMed  Google Scholar 

  33. Nicolai LJ, Ramaekers A, Raemaekers T, Drozdzecki A, Mauss AS, Yan J, et al. Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc Natl Acad Sci U S A 2010, 107: 20553–20558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Feinberg EH, Vanhoven MK, Bendesky A, Wang G, Fetter RD, Shen K, et al. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57: 353–363.

    Article  CAS  PubMed  Google Scholar 

  35. Gordon MD, Scott K. Motor control in a Drosophila taste circuit. Neuron 2009, 61: 373–384.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Shepherd GM. Symposium overview and historical perspective: dendrodendritic synapses: past, present, and future. Ann N Y Acad Sci 2009, 1170: 215–223.

    Article  PubMed  Google Scholar 

  37. Urban NN, Arevian AC. Computing with dendrodendritic synapses in the olfactory bulb. Ann N Y Acad Sci 2009, 1170: 264–269.

    Article  PubMed  Google Scholar 

  38. Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 1995, 14: 341–351.

    Article  CAS  PubMed  Google Scholar 

  39. Nitabach MN, Blau J, Holmes TC. Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 2002, 109: 485–495.

    Article  CAS  PubMed  Google Scholar 

  40. McGuire SE, Roman G, Davis RL. Gene expression systems in Drosophila: a synthesis of time and space. Trends Genet 2004, 20: 384–391.

    Article  CAS  PubMed  Google Scholar 

  41. Nitabach MN, Wu Y, Sheeba V, Lemon WC, Strumbos J, Zelensky PK, et al. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J Neurosci 2006, 26: 479–489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Akerboom J, Carreras Calderon N, Tian L, Wabnig S, Prigge M, Tolo J, et al. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 2013, 6: 2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499: 295–300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Selcho M, Pauls D, El Jundi B, Stocker RF, Thum AS. The role of octopamine and tyramine in Drosophila larval locomotion. J Comp Neurol 2012, 520: 3764–3785.

    Article  CAS  PubMed  Google Scholar 

  45. Yue Fei, Dikai Zhu. Repeated failure in reward pursuit alters innate drosophila larval behaviors. Neurosci Bull 2018, 34(6):901–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Berni J, Pulver SR, Griffith LC, Bate M. Autonomous circuitry for substrate exploration in freely moving Drosophila larvae. Curr Biol 2012, 22: 1861–1870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, et al. Independent optical excitation of distinct neural populations. Nat Methods 2014, 11: 338–346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Saraswati S, Fox LE, Soll DR, Wu CF. Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 2004, 58: 425–441.

    Article  CAS  PubMed  Google Scholar 

  49. Fox LE, Soll DR, Wu CF. Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine beta hydroxlyase mutation. J Neurosci 2006, 26: 1486–1498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kohsaka H, Takasu E, Morimoto T, Nose A. A group of segmental premotor interneurons regulates the speed of axial locomotion in Drosophila larvae. Curr Biol 2014, 24: 2632–2642.

    Article  CAS  PubMed  Google Scholar 

  51. Itakura Y, Kohsaka H, Ohyama T, Zlatic M, Pulver SR, Nose A. Identification of Inhibitory Premotor Interneurons Activated at a Late Phase in a Motor Cycle during Drosophila Larval Locomotion. PLoS One 2015, 10: e0136660.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Matsunaga T, Kohsaka H, Nose A. Gap Junction-Mediated Signaling from Motor Neurons Regulates Motor Generation in the Central Circuits of Larval Drosophila. J Neurosci 2017, 37: 2045–2060.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Prendergast A, Wyart C. Locomotion: Electrical Coupling of Motor and Premotor Neurons. Curr Biol 2016, 26: R235–237.

    Article  CAS  PubMed  Google Scholar 

  54. Song J, Ampatzis K, Bjornfors ER, El Manira A. Motor neurons control locomotor circuit function retrogradely via gap junctions. Nature 2016, 529: 399–402.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Mathieu Louis for sharing free SOS codes; Michael O’Cornor for PTTH-Gal4; Berni Jimena for tsh-Gal80; and Xiaohui Zhang, Chao Tong, Xiaohang Yang, Liming Wang, and Yijun Liu for sharing reagents and valuable discussions. We also thank the Bloomington Drosophila Stock Center and Qinghua Drosophila Stock Center for providing the fly stocks, and the core facilities of Zhejiang University School of Medicine for technical support. This work was supported by grants from the National Basic Research Development Program of China (973 Program, 2013CB945603), the National Natural Science Foundation of China (31070944, 31271147, 31471063, 31671074, and 61572433), the Natural Science Foundation of Zhejiang Province, China (LR13C090001 and LZ14F020002), and the Fundamental Research Funds for the Central Universities, China (2017FZA7003).

Author information

Authors and Affiliations

  1. Department of Neurobiology, Key Laboratory of Medical Neurobiology of the Ministry of Health of China, Key Laboratory of Neurobiology, Zhejiang University School of Medicine, Hangzhou, 310058, China

    Caixia Gong, Weiqiao Zhao, Jie Wang, Kun Li, Peipei Zhou & Zhefeng Gong

  2. Qiushi Academy for Advanced Studies, Zhejiang University, Hangzhou, 310007, China

    Zhenhuan Ouyang & Nenggan Zheng

  3. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, 22011, USA

    Ting Zhao

Authors
  1. Caixia Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenhuan Ouyang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weiqiao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peipei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ting Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nenggan Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhefeng Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Nenggan Zheng or Zhefeng Gong.

Ethics declarations

Conflict of interest

The authors declare no competing interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1132 kb)

Supplementary material 2 (RAR 10193 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gong, C., Ouyang, Z., Zhao, W. et al. A Neuronal Pathway that Commands Deceleration in Drosophila Larval Light-Avoidance. Neurosci. Bull. 35, 959–968 (2019). https://doi.org/10.1007/s12264-019-00349-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-019-00349-w

Keywords

Search

Navigation