Serotonin transporter dependent modulation of food-seeking behavior
Autoři:
Jianzheng He aff001; Franziska Hommen aff001; Nina Lauer aff001; Sophia Balmert aff001; Henrike Scholz aff001
Působiště autorů:
Albertus-Magnus University of Cologne, Department of Biology, Institute for Zoology, Cologne, Germany
aff001
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227554
Souhrn
The olfactory pathway integrates the odor information required to generate correct behavioral responses. To address how changes of serotonin signaling in two contralaterally projecting, serotonin-immunoreactive deutocerebral neurons impacts key odorant attraction in Drosophila melanogaster, we selectively alter serotonin signaling using the serotonin transporter with mutated serotonin binding sites in these neurons and analyzed the consequence on odorant-guided food seeking. The expression of the mutated serotonin transporter selectively changed the odorant attraction in an odorant-specific manner. The shift in attraction was not influenced by more up-stream serotonergic mechanisms mediating behavioral inhibition. The expression of the mutated serotonin transporter in CSD neurons did not influence other behaviors associated with food seeking such as olfactory learning and memory or food consumption. We provide evidence that the change in the attraction by serotonin transporter function might be achieved by increased serotonin signaling and by different serotonin receptors. The 5-HT1B receptor positively regulated the attraction to low and negatively regulated the attraction to high concentrations of acetic acid. In contrast, 5-HT1A and 5-HT2A receptors negatively regulated the attraction in projection neurons to high acetic acid concentrations. These results provide insights into how serotonin signaling in two serotonergic neurons selectively regulates the behavioral response to key odorants during food seeking.
Klíčová slova:
Decision making – Ethanol – Learning and memory – Neurons – Odorants – Olfactory receptor neurons – Serotonin – Serotonin receptors
Zdroje
1. Mehinagic E, Royer G, Symoneaux R, Jourjon F, Prost C. Characterization of odor-active volatiles in apples: influence of cultivars and maturity stage. J Agric Food Chem. 2006;54(7):2678–87. doi: 10.1021/jf052288n 16569061.
2. Alves Z, Melo A, Figueiredo AR, Coimbra MA, Gomes AC, Rocha SM. Exploring the Saccharomyces cerevisiae Volatile Metabolome: Indigenous versus Commercial Strains. PLoS One. 2015;10(11):e0143641. doi: 10.1371/journal.pone.0143641 26600152; PubMed Central PMCID: PMC4657929.
3. Rao MR, Stokes JL. Utilization of ethanol by acetic acid bacteria. J Bacteriol. 1953;66(6):634–8. 13117785; PubMed Central PMCID: PMC317453.
4. Giang T, He J, Belaidi S, Scholz H. Key Odorants Regulate Food Attraction in Drosophila melanogaster. Front Behav Neurosci. 2017;11:160. doi: 10.3389/fnbeh.2017.00160 28928642; PubMed Central PMCID: PMC5591870.
5. Schneider A, Ruppert M, Hendrich O, Giang T, Ogueta M, Hampel S, et al. Neuronal basis of innate olfactory attraction to ethanol in Drosophila. PLoS One. 2012;7(12):e52007. doi: 10.1371/journal.pone.0052007 23284851; PubMed Central PMCID: PMC3527413.
6. Ogueta M, Cibik O, Eltrop R, Schneider A, Scholz H. The influence of Adh function on ethanol preference and tolerance in adult Drosophila melanogaster. Chem Senses. 2010;35(9):813–22. doi: 10.1093/chemse/bjq084 20739429.
7. Silbering AF, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis GS, et al. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci. 2011;31(38):13357–75. doi: 10.1523/JNEUROSCI.2360-11.2011 21940430.
8. Munch D, Galizia CG. DoOR 2.0—Comprehensive Mapping of Drosophila melanogaster Odorant Responses. Sci Rep. 2016;6:21841. doi: 10.1038/srep21841 26912260; PubMed Central PMCID: PMC4766438.
9. Gaudry Q. Serotonergic Modulation of Olfaction in Rodents and Insects. Yale J Biol Med. 2018;91(1):23–32. 29599654; PubMed Central PMCID: PMC5872637.
10. Lizbinski KM, Dacks AM. Intrinsic and Extrinsic Neuromodulation of Olfactory Processing. Front Cell Neurosci. 2017;11:424. doi: 10.3389/fncel.2017.00424 29375314; PubMed Central PMCID: PMC5767172.
11. Ellen CW, Mercer AR. Modulatory actions of dopamine and serotonin on insect antennal lobe neurons: insights from studies in vitro. J Mol Histol. 2012;43(4):401–4. doi: 10.1007/s10735-012-9401-7 22430182.
12. Dacks AM, Christensen TA, Hildebrand JG. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. Journal of Comparative Neurology. 2006;498(6):727–46. doi: 10.1002/cne.21076 WOS:000240356400001. 16927264
13. Roy B, Singh AP, Shetty C, Chaudhary V, North A, Landgraf M, et al. Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system. Neural Dev. 2007;2:20. doi: 10.1186/1749-8104-2-20 17958902; PubMed Central PMCID: PMC2129096.
14. Wilson RI, Mainen ZF. Early events in olfactory processing. Annu Rev Neurosci. 2006;29:163–201. doi: 10.1146/annurev.neuro.29.051605.112950 16776583.
15. Vosshall LB, Stocker RF. Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci. 2007;30:505–33. doi: 10.1146/annurev.neuro.30.051606.094306 17506643.
16. Grabe V, Baschwitz A, Dweck HKM, Lavista-Llanos S, Hansson BS, Sachse S. Elucidating the Neuronal Architecture of Olfactory Glomeruli in the Drosophila Antennal Lobe. Cell Rep. 2016;16(12):3401–13. doi: 10.1016/j.celrep.2016.08.063 27653699.
17. Singh AP, Das RN, Rao G, Aggarwal A, Diegelmann S, Evers JF, et al. Sensory neuron-derived eph regulates glomerular arbors and modulatory function of a central serotonergic neuron. PLoS genetics. 2013;9(4):e1003452. doi: 10.1371/journal.pgen.1003452 23637622; PubMed Central PMCID: PMC3630106.
18. Xu L, He J, Kaiser A, Graber N, Schlager L, Ritze Y, et al. A Single Pair of Serotonergic Neurons Counteracts Serotonergic Inhibition of Ethanol Attraction in Drosophila. PLoS One. 2016;11(12):e0167518. doi: 10.1371/journal.pone.0167518 27936023; PubMed Central PMCID: PMC5147910.
19. Giang T, Ritze Y, Rauchfuss S, Ogueta M, Scholz H. The serotonin transporter expression in Drosophila melanogaster. J Neurogenet. 2011;25(1–2):17–26. doi: 10.3109/01677063.2011.553002 21314480.
20. Dacks AM, Green DS, Root CM, Nighorn AJ, Wang JW. Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J Neurogenet. 2009;23(4):366–77. doi: 10.3109/01677060903085722 19863268; PubMed Central PMCID: PMC2850205.
21. Blenau W, Daniel S, Balfanz S, Thamm M, Baumann A. Dm5-HT2B: Pharmacological Characterization of the Fifth Serotonin Receptor Subtype of Drosophila melanogaster. Front Syst Neurosci. 2017;11:28. doi: 10.3389/fnsys.2017.00028 28553207; PubMed Central PMCID: PMC5425475.
22. Sizemore TR, Dacks AM. Serotonergic Modulation Differentially Targets Distinct Network Elements within the Antennal Lobe of Drosophila melanogaster. Sci Rep. 2016;6:37119. doi: 10.1038/srep37119 27845422; PubMed Central PMCID: PMC5109230.
23. Owald D, Fouquet W, Schmidt M, Wichmann C, Mertel S, Depner H, et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J Cell Biol. 2010;188(4):565–79. doi: 10.1083/jcb.200908055 20176924; PubMed Central PMCID: PMC2828917.
24. Pech U, Pooryasin A, Birman S, Fiala A. Localization of the contacts between Kenyon cells and aminergic neurons in the Drosophila melanogaster brain using SplitGFP reconstitution. J Comp Neurol. 2013;521(17):3992–4026. doi: 10.1002/cne.23388 23784863.
25. Gordon MD, Scott K. Motor control in a Drosophila taste circuit. Neuron. 2009;61(3):373–84. doi: 10.1016/j.neuron.2008.12.033 19217375; PubMed Central PMCID: PMC2650400.
26. Fujioka M, Lear BC, Landgraf M, Yusibova GL, Zhou J, Riley KM, et al. Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development. 2003;130(22):5385–400. doi: 10.1242/dev.00770 13129849; PubMed Central PMCID: PMC2709291.
27. Jackson FR, Newby LM, Kulkarni SJ. Drosophila GABAergic systems: sequence and expression of glutamic acid decarboxylase. Journal of neurochemistry. 1990;54(3):1068–78. doi: 10.1111/j.1471-4159.1990.tb02359.x 1689376.
28. Albin SD, Kaun KR, Knapp JM, Chung P, Heberlein U, Simpson JH. A Subset of Serotonergic Neurons Evokes Hunger in Adult Drosophila. Current biology: CB. 2015;25(18):2435–40. doi: 10.1016/j.cub.2015.08.005 26344091.
29. Lee T, Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 2001;24(5):251–4. doi: 10.1016/s0166-2236(00)01791-4 11311363.
30. Diegelmann S, Bate M, Landgraf M. Gateway cloning vectors for the LexA-based binary expression system in Drosophila. Fly (Austin). 2008;2(4):236–9. doi: 10.4161/fly.6817 18776741; PubMed Central PMCID: PMC2913122.
31. Lai SL, Lee T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci. 2006;9(5):703–9. doi: 10.1038/nn1681 16582903.
32. Sudhakaran IP, Holohan EE, Osman S, Rodrigues V, Vijayraghavan K, Ramaswami M. Plasticity of recurrent inhibition in the Drosophila antennal lobe. J Neurosci. 2012;32(21):7225–31. Epub 2012/05/25. doi: 10.1523/JNEUROSCI.1099-12.2012 22623667.
33. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Gopfert MC, et al. The neural basis of Drosophila gravity-sensing and hearing. Nature. 2009;458(7235):165–71. doi: 10.1038/nature07810 19279630.
34. Tully T, Quinn WG. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A. 1985;157(2):263–77. doi: 10.1007/bf01350033 3939242.
35. 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.
36. Wu Y, Ren Q, Li H, Guo A. The GABAergic anterior paired lateral neurons facilitate olfactory reversal learning in Drosophila. Learn Mem. 2012;19(10):478–86. doi: 10.1101/lm.025726.112 22988290.
37. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, et al. Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A. 2007;104(20):8253–6. doi: 10.1073/pnas.0702726104 17494737; PubMed Central PMCID: PMC1899109.
38. Diegelmann S, Jansen A, Jois S, Kastenholz K, Velo Escarcena L, Strudthoff N, et al. The CApillary FEeder Assay Measures Food Intake in Drosophila melanogaster. J Vis Exp. 2017;(121). doi: 10.3791/55024 28362419.
39. Mahr A, Aberle H. The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns. 2006;6(3):299–309. doi: 10.1016/j.modgep.2005.07.006 16378756.
40. Becher PG, Bengtsson M, Hansson BS, Witzgall P. Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J Chem Ecol. 2010;36(6):599–607. doi: 10.1007/s10886-010-9794-2 20437263.
41. Zhu J, Park KC, Baker TC. Identification of odors from overripe mango that attract vinegar flies, Drosophila melanogaster. J Chem Ecol. 2003;29(4):899–909. doi: 10.1023/a:1022931816351 12775150.
42. Coates KE, Majot AT, Zhang X, Michael CT, Spitzer SL, Gaudry Q, et al. Identified Serotonergic Modulatory Neurons Have Heterogeneous Synaptic Connectivity within the Olfactory System of Drosophila. J Neurosci. 2017;37(31):7318–31. doi: 10.1523/JNEUROSCI.0192-17.2017 28659283; PubMed Central PMCID: PMC5546105.
43. Zhou S, Stone EA, Mackay TF, Anholt RR. Plasticity of the chemoreceptor repertoire in Drosophila melanogaster. PLoS genetics. 2009;5(10):e1000681. doi: 10.1371/journal.pgen.1000681 19816562; PubMed Central PMCID: PMC2750752.
44. Zhang X, Gaudry Q. Functional integration of a serotonergic neuron in the Drosophila antennal lobe. Elife. 2016;5. doi: 10.7554/eLife.16836 27572257; PubMed Central PMCID: PMC5030083.
45. 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(47):20553–8. doi: 10.1073/pnas.1010198107 21059961; PubMed Central PMCID: PMC2996714.
46. Davis RL. SnapShot: Olfactory Classical Conditioning of Drosophila. Cell. 2015;163(2):524–e1. doi: 10.1016/j.cell.2015.09.043 26451491.
47. Bracker LB, Siju KP, Varela N, Aso Y, Zhang M, Hein I, et al. Essential role of the mushroom body in context-dependent CO(2) avoidance in Drosophila. Current biology: CB. 2013;23(13):1228–34. doi: 10.1016/j.cub.2013.05.029 23770186.
48. Ko KI, Root CM, Lindsay SA, Zaninovich OA, Shepherd AK, Wasserman SA, et al. Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits. Elife. 2015;4. doi: 10.7554/eLife.08298 26208339; PubMed Central PMCID: PMC4531282.
49. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenbock G. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron. 2002;36(3):463–74. doi: 10.1016/s0896-6273(02)00975-3 12408848.
50. 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. Current biology: CB. 2006;16(17):1741–7. doi: 10.1016/j.cub.2006.07.023 16950113.
51. Semmelhack JL, Wang JW. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature. 2009;459(7244):218–23. doi: 10.1038/nature07983 19396157; PubMed Central PMCID: PMC2702439.
52. Ai M, Min S, Grosjean Y, Leblanc C, Bell R, Benton R, et al. Acid sensing by the Drosophila olfactory system. Nature. 2010;468(7324):691–5. doi: 10.1038/nature09537 21085119; PubMed Central PMCID: PMC3105465.
53. Saudou F, Boschert U, Amlaiky N, Plassat JL, Hen R. A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. EMBO J. 1992;11(1):7–17. 1310937; PubMed Central PMCID: PMC556419.
54. Tanaka NK, Endo K, Ito K. Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain. J Comp Neurol. 2012;520(18):4067–130. doi: 10.1002/cne.23142 22592945.
55. Wang K, Gong J, Wang Q, Li H, Cheng Q, Liu Y, et al. Parallel pathways convey olfactory information with opposite polarities in Drosophila. Proc Natl Acad Sci U S A. 2014;111(8):3164–9. doi: 10.1073/pnas.1317911111 24516124; PubMed Central PMCID: PMC3939862.
56. Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science. 2011;334(6056):670–4. doi: 10.1126/science.1212782 22053049.
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Je libo čepici místo mozkového implantátu?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy