#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Dopaminergic D2-Like Receptors Delimit Recurrent Cholinergic-Mediated Motor Programs during a Goal-Oriented Behavior


Caenorhabditis elegans male copulation requires coordinated temporal-spatial execution of different motor outputs. During mating, a cloacal circuit consisting of cholinergic sensory-motor neurons and sex muscles maintains the male's position and executes copulatory spicule thrusts at his mate's vulva. However, distinct signaling mechanisms that delimit these behaviors to their proper context are unclear. We found that dopamine (DA) signaling directs copulatory spicule insertion attempts to the hermaphrodite vulva by dampening spurious stimulus-independent sex muscle contractions. From pharmacology and genetic analyses, DA antagonizes stimulatory ACh signaling via the D2-like receptors, DOP-2 and DOP-3, and Gαo/i proteins, GOA-1 and GPA-7. Calcium imaging and optogenetics suggest that heightened DA-expressing ray neuron activities coincide with the cholinergic cloacal ganglia function during spicule insertion attempts. D2-like receptor signaling also attenuates the excitability of additional mating circuits to reduce the duration of mating attempts with unproductive and/or inappropriate partners. This suggests that, during wild-type mating, simultaneous DA-ACh signaling modulates the activity threshold of repetitive motor programs, thus confining the behavior to the proper situational context.


Vyšlo v časopise: Dopaminergic D2-Like Receptors Delimit Recurrent Cholinergic-Mediated Motor Programs during a Goal-Oriented Behavior. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003015
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003015

Souhrn

Caenorhabditis elegans male copulation requires coordinated temporal-spatial execution of different motor outputs. During mating, a cloacal circuit consisting of cholinergic sensory-motor neurons and sex muscles maintains the male's position and executes copulatory spicule thrusts at his mate's vulva. However, distinct signaling mechanisms that delimit these behaviors to their proper context are unclear. We found that dopamine (DA) signaling directs copulatory spicule insertion attempts to the hermaphrodite vulva by dampening spurious stimulus-independent sex muscle contractions. From pharmacology and genetic analyses, DA antagonizes stimulatory ACh signaling via the D2-like receptors, DOP-2 and DOP-3, and Gαo/i proteins, GOA-1 and GPA-7. Calcium imaging and optogenetics suggest that heightened DA-expressing ray neuron activities coincide with the cholinergic cloacal ganglia function during spicule insertion attempts. D2-like receptor signaling also attenuates the excitability of additional mating circuits to reduce the duration of mating attempts with unproductive and/or inappropriate partners. This suggests that, during wild-type mating, simultaneous DA-ACh signaling modulates the activity threshold of repetitive motor programs, thus confining the behavior to the proper situational context.


Zdroje

1. BeaulieuJM, SotnikovaTD, MarionS, LefkowitzRJ, GainetdinovRR, et al. (2005) An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122: 261–273.

2. FienbergAA, HiroiN, MermelsteinPG, SongW, SnyderGL, et al. (1998) DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 281: 838–842.

3. YanZ, Hsieh-WilsonL, FengJ, TomizawaK, AllenPB, et al. (1999) Protein phosphatase 1 modulation of neostriatal AMPA channels: regulation by DARPP-32 and spinophilin. Nat Neurosci 2: 13–17.

4. WittenIB, LinSC, BrodskyM, PrakashR, DiesterI, et al. (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330: 1677–1681.

5. BeaulieuJM, SotnikovaTD, YaoWD, KockeritzL, WoodgettJR, et al. (2004) Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci U S A 101: 5099–5104.

6. YanZ, SurmeierDJ (1997) D5 dopamine receptors enhance Zn2+-sensitive GABA(A) currents in striatal cholinergic interneurons through a PKA/PP1 cascade. Neuron 19: 1115–1126.

7. GraybielAM, AosakiT, FlahertyAW, KimuraM (1994) The basal ganglia and adaptive motor control. Science 265: 1826–1831.

8. SmithY, BevanMD, ShinkE, BolamJP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86: 353–387.

9. WangZ, KaiL, DayM, RonesiJ, YinHH, et al. (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50: 443–452.

10. DengP, ZhangY, XuZC (2007) Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons. J Neurosci 27: 3148–3156.

11. MorrisG, ArkadirD, NevetA, VaadiaE, BergmanH (2004) Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43: 133–143.

12. CalabresiP, PicconiB, ParnettiL, Di FilippoM (2006) A convergent model for cognitive dysfunctions in Parkinson's disease: the critical dopamine-acetylcholine synaptic balance. Lancet Neurol 5: 974–983.

13. DingJ, GuzmanJN, TkatchT, ChenS, GoldbergJA, et al. (2006) RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion. Nat Neurosci 9: 832–842.

14. PisaniA, BernardiG, DingJ, SurmeierDJ (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci 30: 545–553.

15. RazA, Frechter-MazarV, FeingoldA, AbelesM, VaadiaE, et al. (2001) Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys. J Neurosci 21: RC128.

16. SulstonJ, DewM, BrennerS (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 163: 215–226.

17. Vidal-GadeaA, TopperS, YoungL, CrispA, KressinL, et al. (2011) Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin. Proc Natl Acad Sci U S A 108: 17504–17509.

18. RoseJK, RankinCH (2001) Analyses of habituation in Caenorhabditis elegans. Learn Mem 8: 63–69.

19. SanyalS, WintleRF, KindtKS, NuttleyWM, ArvanR, et al. (2004) Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J 23: 473–482.

20. SugiuraM, FukeS, SuoS, SasagawaN, Van TolHH, et al. (2005) Characterization of a novel D2-like dopamine receptor with a truncated splice variant and a D1-like dopamine receptor unique to invertebrates from Caenorhabditis elegans. J Neurochem 94: 1146–1157.

21. ChaseDL, PepperJS, KoelleMR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7: 1096–1103.

22. SawinER, RanganathanR, HorvitzHR (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26: 619–631.

23. AllenAT, MaherKN, WaniKA, BettsKE, ChaseDL (2011) Coexpressed D1- and D2-like dopamine receptors antagonistically modulate acetylcholine release in Caenorhabditis elegans. Genetics 188: 579–590.

24. LiuY, LeBeoufB, GuoX, CorreaPA, GualbertoDG, et al. (2011) A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditis elegans male copulation. PLoS Genet 7: e1001326 doi:10.1371/journal.pgen.1001326.

25. GarciaLR, MehtaP, SternbergPW (2001) Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 107: 777–788.

26. KooPK, BianX, SherlekarAL, BunkersMR, LintsR (2011) The robustness of Caenorhabditis elegans male mating behavior depends on the distributed properties of ray sensory neurons and their output through core and male-specific targets. J Neurosci 31: 7497–7510.

27. LiuKS, SternbergPW (1995) Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14: 79–89.

28. LiuY, LeBoeufB, GarciaLR (2007) G alpha(q)-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditis elegans mating behavior. J Neurosci 27: 1411–1421.

29. GarciaLR, SternbergPW (2003) Caenorhabditis elegans UNC-103 ERG-like potassium channel regulates contractile behaviors of sex muscles in males before and during mating. J Neurosci 23: 2696–2705.

30. LeBoeufB, GuoX, GarciaLR (2011) The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K+ channels in C. elegans males. Neuroscience 175: 1–17.

31. GruningerTR, GualbertoDG, GarciaLR (2008) Sensory perception of food and insulin-like signals influence seizure susceptibility. PLoS Genet 4: e1000117 doi:10.1371/journal.pgen.1000117.

32. GruningerTR, GualbertoDG, LeBoeufB, GarciaLR (2006) Integration of male mating and feeding behaviors in Caenorhabditis elegans. J Neurosci 26: 169–179.

33. LeBoeufB, GruningerTR, GarciaLR (2007) Food deprivation attenuates seizures through CaMKII and EAG K+ channels. PLoS Genet 3: e156 doi:10.1371/journal.pgen.0030156.

34. LoerCM, KenyonCJ (1993) Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13: 5407–5417.

35. BarriosA, NurrishS, EmmonsSW (2008) Sensory regulation of C. elegans male mate-searching behavior. Curr Biol 18: 1865–1871.

36. SrinivasanJ, KaplanF, AjrediniR, ZachariahC, AlbornHT, et al. (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454: 1115–1118.

37. WhittakerAJ, SternbergPW (2009) Coordination of opposing sex-specific and core muscle groups regulates male tail posture during Caenorhabditis elegans male mating behavior. BMC Biol 7: 33.

38. WhiteJQ, NicholasTJ, GrittonJ, TruongL, DavidsonER, et al. (2007) The sensory circuitry for sexual attraction in C. elegans males. Curr Biol 17: 1847–1857.

39. LiuT, KimK, LiC, BarrMM (2007) FMRFamide-like neuropeptides and mechanosensory touch receptor neurons regulate male sexual turning behavior in Caenorhabditis elegans. J Neurosci 27: 7174–7182.

40. SchindelmanG, WhittakerAJ, ThumJY, GharibS, SternbergPW (2006) Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord. BMC Biol 4: 26.

41. O'HaganR, PiaseckiBP, SilvaM, PhirkeP, NguyenKC, et al. (2011) The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol 21: 1685–1694.

42. PetersenCI, McFarlandTR, StepanovicSZ, YangP, ReinerDJ, et al. (2004) In vivo identification of genes that modify ether-a-go-go-related gene activity in Caenorhabditis elegans may also affect human cardiac arrhythmia. Proc Natl Acad Sci U S A 101: 11773–11778.

43. McDonaldPW, HardieSL, JessenTN, CarvelliL, MatthiesDS, et al. (2007) Vigorous motor activity in Caenorhabditis elegans requires efficient clearance of dopamine mediated by synaptic localization of the dopamine transporter DAT-1. J Neurosci 27: 14216–14227.

44. StegerKA, AveryL (2004) The GAR-3 muscarinic receptor cooperates with calcium signals to regulate muscle contraction in the Caenorhabditis elegans pharynx. Genetics 167: 633–643.

45. EzcurraM, TanizawaY, SwobodaP, SchaferWR (2011) Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling. EMBO J 30: 1110–1122.

46. RingstadN, AbeN, HorvitzHR (2009) Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science 325: 96–100.

47. JansenG, ThijssenKL, WernerP, van der HorstM, HazendonkE, et al. (1999) The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat Genet 21: 414–419.

48. BringmannH, CowanCR, KongJ, HymanAA (2007) LET-99, GOA-1/GPA-16, and GPR-1/2 are required for aster-positioned cytokinesis. Curr Biol 17: 185–191.

49. SuoS, SasagawaN, IshiuraS (2003) Cloning and characterization of a Caenorhabditis elegans D2-like dopamine receptor. J Neurochem 86: 869–878.

50. JarrellTA, WangY, BloniarzAE, BrittinCA, XuM, et al. (2012) The connectome of a decision-making neural network. Science 337: 437–444.

51. ChasnovJR, SoWK, ChanCM, ChowKL (2007) The species, sex, and stage specificity of a Caenorhabditis sex pheromone. Proc Natl Acad Sci U S A 104: 6730–6735.

52. PandeyP, HarbinderS (2012) The Caenorhabditis elegans D2-like dopamine receptor DOP-2 physically interacts with GPA-14, a G-alpha-i subunit. J Mol Signal 7: 3.

53. Hernandez-LopezS, TkatchT, Perez-GarciE, GalarragaE, BargasJ, et al. (2000) D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3-calcineurin-signaling cascade. J Neurosci 20: 8987–8995.

54. BateupHS, SantiniE, ShenW, BirnbaumS, ValjentE, et al. (2010) Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci U S A 107: 14845–14850.

55. StoofJC, KebabianJW (1981) Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum. Nature 294: 366–368.

56. LintsR, JiaL, KimK, LiC, EmmonsSW (2004) Axial patterning of C. elegans male sensilla identities by selector genes. Dev Biol 269: 137–151.

57. MauriceN, MercerJ, ChanCS, Hernandez-LopezS, HeldJ, et al. (2004) D2 dopamine receptor-mediated modulation of voltage-dependent Na+ channels reduces autonomous activity in striatal cholinergic interneurons. J Neurosci 24: 10289–10301.

58. BateupHS, SvenningssonP, KuroiwaM, GongS, NishiA, et al. (2008) Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat Neurosci 11: 932–939.

59. BagettaV, PicconiB, MarinucciS, SgobioC, PendolinoV, et al. (2011) Dopamine-dependent long-term depression is expressed in striatal spiny neurons of both direct and indirect pathways: implications for Parkinson's disease. J Neurosci 31: 12513–12522.

60. CalabresiP, MajR, MercuriNB, BernardiG (1992) Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 142: 95–99.

61. PicconiB, CentonzeD, HakanssonK, BernardiG, GreengardP, et al. (2003) Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 6: 501–506.

62. ShenW, FlajoletM, GreengardP, SurmeierDJ (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321: 848–851.

63. ReinerDJ, WeinshenkerD, TianH, ThomasJH, NishiwakiK, et al. (2006) Behavioral genetics of caenorhabditis elegans unc-103-encoded erg-like K(+) channel. J Neurogenet 20: 41–66.

64. TianL, HiresSA, MaoT, HuberD, ChiappeME, et al. (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875–881.

65. GranatoM, SchnabelH, SchnabelR (1994) pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res 22: 1762–1763.

66. GuoX, NavettaA, GualbertoDG, GarciaLR (2012) Behavioral decay in aging male C. elegans correlates with increased cell excitability. Neurobiol Aging

67. KamathRS, Martinez-CamposM, ZipperlenP, FraserAG, AhringerJ (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

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#