Modulations of microbehaviour by associative memory strength in Drosophila larvae

Autoři: Michael Thane aff001;  Vignesh Viswanathan aff001;  Tessa Christin Meyer aff001;  Emmanouil Paisios aff001;  Michael Schleyer aff001
Působiště autorů: Leibniz Institute for Neurobiology (LIN), Department Genetics of Learning and Memory, Magdeburg, Germany aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Finding food is a vital skill and a constant task for any animal, and associative learning of food-predicting cues gives an advantage in this daily struggle. The strength of the associations between cues and food depends on a number of parameters, such as the salience of the cue, the strength of the food reward and the number of joint cue-food experiences. We investigate what impact the strength of an associative odour-sugar memory has on the microbehaviour of Drosophila melanogaster larvae. We find that larvae form stronger memories with increasing concentrations of sugar or odour, and that these stronger memories manifest themselves in stronger modulations of two aspects of larval microbehaviour, the rate and the direction of lateral reorientation manoeuvres (so-called head casts). These two modulations of larval behaviour are found to be correlated to each other in every experiment performed, which is in line with a model that assumes that both modulations are controlled by a common motor output. Given that the Drosophila larva is a genetically tractable model organism that is well suited to the study of simple circuits at the single-cell level, these analyses can guide future research into the neuronal circuits underlying the translation of associative memories of different strength into behaviour, and may help to understand how these processes are organised in more complex systems.

Klíčová slova:

Animal behavior – Animal performance – Collective animal behavior – Drosophila melanogaster – Larvae – Learning – Memory – Neurons


1. Gerber B, Stocker RF, Tanimura T, Thum AS. Smelling, tasting, learning: Drosophila as a study case. Results Probl Cell Differ. 2009;47: 139–85. doi: 10.1007/400_2008_9 19145411

2. Diegelmann S, Klagges B, Michels B, Schleyer M, Gerber B. Maggot learning and Synapsin function. J Exp Biol. 2013;216(Pt 6): 939–51. doi: 10.1242/jeb.076208 23447663

3. Schleyer M, Diegelmann S, Michels B, Saumweber T, Gerber B. 'Decision-making' in larval Drosophila. In: Menzel R, Benjamin P, editors. Invertebrate Learning and Memory. München: Elsevier; 2013. p. 41–55.

4. Widmann A, Eichler K, Selcho M, Thum AS, Pauls D. Odor-taste learning in Drosophila larvae. J Insect Physiol. 2018;106(Pt 1): 47–54. doi: 10.1016/j.jinsphys.2017.08.004 28823531

5. Schipanski A, Yarali A, Niewalda T, Gerber B. Behavioral analyses of sugar processing in choice, feeding, and learning in larval Drosophila. Chem Sens. 2008;33(6): 563–73.

6. Rohwedder A, Pfitzenmaier JE, Ramsperger N, Apostolopoulou AA, Widmann A, Thum AS. Nutritional value-dependent and nutritional value-independent effects on Drosophila melanogaster larval behavior. Chem Sens. 2012;37(8): 711–21.

7. Mishra D, Chen YC, Yarali A, Oguz T, Gerber B. Olfactory memories are intensity specific in larval Drosophila. J Exp Biol. 2013;216(Pt 9): 1552–60. doi: 10.1242/jeb.082222 23596280

8. Neuser K, Husse J, Stock P, Gerber B. Appetitive olfactory learning in Drosophila larvae: effects of repetition, reward strength, age, gender, assay type and memory span. Anim Behav. 2005;69: 891–8.

9. Weiglein A, Gerstner F, Mancini N, Schleyer M, Gerber B. One-trial learning in larval Drosophila. Learn Mem. 2019;26(4): 109–20. doi: 10.1101/lm.049106.118 30898973

10. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci. 2003;23(33):10495–502. doi: 10.1523/JNEUROSCI.23-33-10495.2003 14627633

11. Colomb J, Kaiser L, Chabaud MA, Preat T. Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Gen Brain Behav. 2009;8(4):407–15.

12. Niewalda T, Voller T, Eschbach C, Ehmer J, Chou WC, Timme M, et al. A combined perceptual, physico-chemical, and imaging approach to 'odour-distances' suggests a categorizing function of the Drosophila antennal lobe. PloS one. 2011;6(9):e24300. doi: 10.1371/journal.pone.0024300 21931676

13. Scherer S, Stocker RF, Gerber B. Olfactory learning in individually assayed Drosophila larvae. Learn Mem. 2003;10(3): 217–25. doi: 10.1101/lm.57903 12773586

14. Saumweber T, Husse J, Gerber B. Innate attractiveness and associative learnability of odors can be dissociated in larval Drosophila. Chem Sens. 2011;36(3): 223–35.

15. Kleber J, Chen YC, Michels B, Saumweber T, Schleyer M, Kahne T, et al. Synapsin is required to "boost" memory strength for highly salient events. Learn Mem. 2016;23(1): 9–20. doi: 10.1101/lm.039685.115 26670182

16. Schleyer M, Miura D, Tanimura T, Gerber B. Learning the specific quality of taste reinforcement in larval Drosophila. eLife. 2015;4.

17. Schleyer M, Reid SF, Pamir E, Saumweber T, Paisios E, Davies A, et al. The impact of odor-reward memory on chemotaxis in larval Drosophila. Learn Mem. 2015;22(5): 267–77. doi: 10.1101/lm.037978.114 25887280

18. Paisios E, Rjosk A, Pamir E, Schleyer M. Common microbehavioral "footprint" of two distinct classes of conditioned aversion. Learn Mem. 2017;24(5): 191–8. doi: 10.1101/lm.045062.117 28416630

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

20. 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(8): e23180. doi: 10.1371/journal.pone.0023180 21858019

21. 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(3): 290–6. doi: 10.1038/nmeth.1853 22245808

22. Davies A, Louis M, Webb B. A model of Drosophila larva chemotaxis. PLoS Comp Biol. 2015;11(11):e1004606.

23. Schulze A, Gomez-Marin A, Rajendran VG, Lott G, Musy M, Ahammad P, et al. Dynamical feature extraction at the sensory periphery guides chemotaxis. eLife. 2015;4.

24. Gomez-Marin A, Louis M. Active sensation during orientation behavior in the Drosophila larva: more sense than luck. Curr Op Neurobiol. 2012;22(2):208–15. doi: 10.1016/j.conb.2011.11.008 22169055

25. Gomez-Marin A, Louis M. Multilevel control of run orientation in Drosophila larval chemotaxis. Front Behav Neurosci. 2014;8:38. doi: 10.3389/fnbeh.2014.00038 24592220

26. Wystrach A, Lagogiannis K, Webb B. Continuous lateral oscillations as a core mechanism for taxis in Drosophila larvae. eLife. 2016;5.

27. Loveless J, Webb B. A neuromechanical model of larval chemotaxis. Integr Comp Biol. 2018;58(5):906–14. doi: 10.1093/icb/icy094 30060198

28. Michels B, Saumweber T, Biernacki R, Thum J, Glasgow RDV, Schleyer M, et al. Pavlovian conditioning of larval Drosophila: An illustrated, multilingual, hands-on manual for odor-taste associative learning in maggots. Front Behav Neurosci. 2017;11: 45. doi: 10.3389/fnbeh.2017.00045 28469564

29. Holm S. A simple sequentially rejective multiple test procedure. Scand J Statist. 1979;6(2):65–70.

30. Thum AS, Gerber B. Connectomics and function of a memory network: the mushroom body of larval Drosophila. Curr Opin Neurobiol. 2019;54: 146–54. doi: 10.1016/j.conb.2018.10.007 30368037

31. Heisenberg M. Mushroom body memoir: from maps to models. Nature Rev. 2003;4(4):266–75.

32. Guven-Ozkan T, Davis RL. Functional neuroanatomy of Drosophila olfactory memory formation. Learn Mem. 2014;21(10):519–26. doi: 10.1101/lm.034363.114 25225297

33. Cognigni P, Felsenberg J, Waddell S. Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila. Curr Opin Neurobiol. 2018;49:51–8. doi: 10.1016/j.conb.2017.12.002 29258011

34. Tumkaya T, Ott S, Claridge-Chang A. A systematic review of Drosophila short-term-memory genetics: Meta-analysis reveals robust reproducibility. Neurosci Biobehav Rev. 2018;95:361–82. doi: 10.1016/j.neubiorev.2018.07.016 30077573

35. Horiuchi J. Recurrent loops: Incorporating prediction error and semantic/episodic theories into Drosophila associative memory models. Genes, brain, and behavior. 2019:e12567. doi: 10.1111/gbb.12567 30891930

36. Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, Erbguth K, et al. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol. 2006;16(17):1741–7. doi: 10.1016/j.cub.2006.07.023 16950113

37. Rohwedder A, Wenz NL, Stehle B, Huser A, Yamagata N, Zlatic M, et al. Four individually identified paired dopamine neurons signal reward in larval Drosophila. Curr Biol. 2016;26(5): 661–9. doi: 10.1016/j.cub.2016.01.012 26877086

38. Eichler K, Li F, Litwin-Kumar A, Park Y, Andrade I, Schneider-Mizell CM, et al. The complete connectome of a learning and memory centre in an insect brain. Nature. 2017;548(7666): 175–82. doi: 10.1038/nature23455 28796202

39. Saumweber T, Rohwedder A, Schleyer M, Eichler K, Chen YC, Aso Y, et al. Functional architecture of reward learning in mushroom body extrinsic neurons of larval Drosophila. Nat Comm. 2018;9(1): 1104.

40. Liu C, Placais PY, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, et al. A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature. 2012;488(7412):512–6. doi: 10.1038/nature11304 22810589

41. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, et al. Layered reward signalling through octopamine and dopamine in Drosophila. Nature. 2012;492(7429):433–7. doi: 10.1038/nature11614 23103875

42. Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, et al. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife. 2014a;3:e04577. doi: 10.7554/eLife.04577 25535793

43. Aso Y, Rubin GM. Dopaminergic neurons write and update memories with cell-type-specific rules. eLife. 2016;5.

44. Takemura SY, Aso Y, Hige T, Wong A, Lu Z, Xu CS, et al. A connectome of a learning and memory center in the adult Drosophila brain. eLife. 2017;6.

45. Sejourne J, Placais PY, Aso Y, Siwanowicz I, Trannoy S, Thoma V, et al. Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat Neurosci. 2011;14(7):903–10. doi: 10.1038/nn.2846 21685917

46. Placais PY, Trannoy S, Friedrich AB, Tanimoto H, Preat T. Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila. Cell Rep. 2013;5(3):769–80. doi: 10.1016/j.celrep.2013.09.032 24209748

47. Hige T, Aso Y, Modi MN, Rubin GM, Turner GC. Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila. Neuron. 2015;88(5):985–98. doi: 10.1016/j.neuron.2015.11.003 26637800

48. Cohn R, Morantte I, Ruta V. Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila. Cell. 2015;163(7): 1742–55. doi: 10.1016/j.cell.2015.11.019 26687359

49. Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K, Belliart-Guerin G, et al. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife. 2014;3: e04580. doi: 10.7554/eLife.04580 25535794

50. Owald D, Felsenberg J, Talbot CB, Das G, Perisse E, Huetteroth W, et al. Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila. Neuron. 2015;86(2): 417–27. doi: 10.1016/j.neuron.2015.03.025 25864636

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2019 Číslo 10
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