#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability


Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.


Vyšlo v časopise: Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002768
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002768

Souhrn

Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.


Zdroje

1. FrostWNCastellucciVFHawkinsRDKandelER 1985 Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc Natl Acad Sci U S A 82 8266 8269

2. MedinaJFRepaJCMaukMDLeDouxJE 2002 Parallels between cerebellum- and amygdala-dependent conditioning. Nat Rev Neurosci 3 122 131

3. McGuireSEDeshazerMDavisRL 2005 Thirty years of olfactory learning and memory research in Drosophila melanogaster. Progress in neurobiology Prog Neurobiol 76 328 347

4. HeisenbergM 2003 Mushroom body memoir: from maps to models. Nat Rev Neurosci 4 266 275

5. GerberBTanimotoHHeisenbergM 2004 An engram found? Evaluating the evidence from fruit flies. Curr Opin Neurobiol 14 737 744

6. KeeneACWaddellS 2007 Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8 341 354

7. ZarsTFischerMSchulzRHeisenbergM 2000 Localization of a short-term memory in Drosophila. Science 288 672 675

8. GervasiNTchenioPPréatT 2010 PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65 516 529

9. TomchikSMDavisRL 2009 Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64 510 521

10. WangYGuoHFPologrutoTAHannanFHakkerI 2004 Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J Neurosci 24 6507 6514

11. TurnerGCBazhenovMLaurentG 2008 Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99 734 746

12. HoneggerKSCampbellRATurnerGC 2011 Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J Neurosci 31 11772 11785

13. CrittendenJRSkoulakisEMHanKAKalderonDDavisRL 1998 Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5 38 51

14. LinHHLaiJSChinALChenYCChiangAS 2007 A map of olfactory representation in the Drosophila mushroom body. Cell 128 1205 1217

15. TanakaNKTanimotoHItoK 2008 Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508 711 755

16. AsoYGrübelKBuschSFriedrichABSiwanowiczI 2009 The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23 156 172

17. KimYCLeeHGHanKA 2007 D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J Neurosci 27 7640 7647

18. QinHCressyMLiWCoravosJSIzziSA 2012 Gamma Neurons Mediate Dopaminergic Input during Aversive Olfactory Memory Formation in Drosophila. Curr Biol

19. Claridge-ChangARoordaRDVrontouESjulsonLLiH 2009 Writing memories with light-addressable reinforcement circuitry. Cell 139 405 415

20. SchrollCRiemenspergerTBucherDEhmerJVöllerT 2006 Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16 1741 1747

21. MaoZDavisRL 2009 Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3 5

22. NässelDRElekesK 1992 Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res 267 147 167

23. WhiteKEHumphreyDMHirthF 2010 The dopaminergic system in the aging brain of Drosophila. Front Neurosci 4 205

24. RiemenspergerTVöllerTStockPBuchnerEFialaA 2005 Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15 1953 1960

25. AsoYSiwanowiczIBräckerLItoKKitamotoT 2010 Specific Dopaminergic Neurons for the Formation of Labile Aversive Memory. Curr Biol 20 1445 1451

26. KrashesMJDasGuptaSVreedeAWhiteBArmstrongJD 2009 A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139 416 427

27. ZhangKGuoJZPengYXiWGuoA 2007 Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila. Science 316 1901 1904

28. BangSHyunSHongSTKangJJeongK 2011 Dopamine signalling in mushroom bodies regulates temperature-preference behaviour in Drosophila. PLoS Genet 7 e1001346 doi:10.1371/journal.pgen.1001346

29. KaunKRAzanchiRMaungZHirshJHeberleinU 2011 A Drosophila model for alcohol reward. Nat Neurosci 14 612 619

30. BlumALLiWCressyMDubnauJ 2009 Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr Biol 19 1341 1350

31. AkalalDBWilsonCFZongLTanakaNKItoK 2006 Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn Mem 13 659 668

32. IsabelGPascualAPreatT 2004 Exclusive consolidated memory phases in Drosophila. Science 304 1024 1027

33. KrashesMJKeeneACLeungBArmstrongJDWaddellS 2007 Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53 103 115

34. HamadaFNRosenzweigMKangKPulverSRGhezziA 2008 An internal thermal sensor controlling temperature preference in Drosophila. Nature 454 217 220

35. SitaramanDZarsMLaferriereHChenYCSable-SmithA 2008 Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci U S A 105 5579 5584

36. KitamotoTIkedaKSalvaterraPM 1995 Regulation of choline acetyltransferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J Neurobiol 28 70 81

37. LiHChaneySRobertsIJForteMHirshJ 2000 Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 10 211 214

38. LeePTLinHWChangYHFuTFDubnauJ 2011 Serotonin-mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila. Proc Natl Acad Sci U S A 108 13794 13799

39. YuDKeeneACSrivatsanAWaddellSDavisRL 2005 Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123 945 957

40. PascualAPreatT 2001 Localization of long-term memory within the Drosophila mushroom body. Science 294 1115 1117

41. YuDAkalalDBDavisRL 2006 Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52 845 855

42. SéjournéJPlaçaisPYAsoYSiwanowiczITrannoyS 2011 Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila. Nat Neurosci 14 903 910

43. KleinSStaringMMurphyKViergeverMAPluimJP 2010 elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging 29 196 205

44. KitamotoT 2001 Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47 81 92

45. SchwaerzelMMonastiriotiMScholzHFriggi-GrelinFBirmanS 2003 Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23 10495 10502

46. RiemenspergerTIsabelGCoulomHNeuserKSeugnetL 2011 Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. Proc Natl Acad Sci U S A 108 834 839

47. SchwaerzelMHeisenbergMZarsT 2002 Extinction antagonizes olfactory memory at the subcellular level. Neuron 35 951 960

48. SherffCMCarewTJ 1999 Coincident induction of long-term facilitation in Aplysia: cooperativity between cell bodies and remote synapses. Science 285 1911 1914

49. WuCLShihMFLaiJSYangHTTurnerGC 2011 Heterotypic gap junctions between two neurons in the drosophila brain are critical for memory. Curr Biol 21 848 854

50. PitmanJLHuetterothWBurkeCJKrashesMJLaiSL 2011 A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body. Curr Biol 21 855 861

51. PlaçaisPYTrannoySIsabelGAsoYSiwanowiczI 2012 Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila. Nat Neurosci 15 592 599

52. McGuireSELePTOsbornAJMatsumotoKDavisRL 2003 Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302 1765 1768

53. TullyTQuinnWG 1985 Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157 263 277

54. ThumASJenettAItoKHeisenbergMTanimotoH 2007 Multiple memory traces for olfactory reward learning in Drosophila. J Neurosci 27 11132 11138

55. RasbandWS 1997–2011 ImageJ, U.S.: National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#