A Cholinergic-Regulated Circuit Coordinates the Maintenance and Bi-Stable States of a Sensory-Motor Behavior during Male Copulation


Penetration of a male copulatory organ into a suitable mate is a conserved and necessary behavioral step for most terrestrial matings; however, the detailed molecular and cellular mechanisms for this distinct social interaction have not been elucidated in any animal. During mating, the Caenorhabditis elegans male cloaca is maintained over the hermaphrodite's vulva as he attempts to insert his copulatory spicules. Rhythmic spicule thrusts cease when insertion is sensed. Circuit components consisting of sensory/motor neurons and sex muscles for these steps have been previously identified, but it was unclear how their outputs are integrated to generate a coordinated behavior pattern. Here, we show that cholinergic signaling between the cloacal sensory/motor neurons and the posterior sex muscles sustains genital contact between the sexes. Simultaneously, via gap junctions, signaling from these muscles is transmitted to the spicule muscles, thus coupling repeated spicule thrusts with vulval contact. To transit from rhythmic to sustained muscle contraction during penetration, the SPC sensory-motor neurons integrate the signal of spicule's position in the vulva with inputs from the hook and cloacal sensilla. The UNC-103 K+ channel maintains a high excitability threshold in the circuit, so that sustained spicule muscle contraction is not stimulated by fewer inputs. We demonstrate that coordination of sensory inputs and motor outputs used to initiate, maintain, self-monitor, and complete an innate behavior is accomplished via the coupling of a few circuit components.


Vyšlo v časopise: A Cholinergic-Regulated Circuit Coordinates the Maintenance and Bi-Stable States of a Sensory-Motor Behavior during Male Copulation. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001326
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001326

Souhrn

Penetration of a male copulatory organ into a suitable mate is a conserved and necessary behavioral step for most terrestrial matings; however, the detailed molecular and cellular mechanisms for this distinct social interaction have not been elucidated in any animal. During mating, the Caenorhabditis elegans male cloaca is maintained over the hermaphrodite's vulva as he attempts to insert his copulatory spicules. Rhythmic spicule thrusts cease when insertion is sensed. Circuit components consisting of sensory/motor neurons and sex muscles for these steps have been previously identified, but it was unclear how their outputs are integrated to generate a coordinated behavior pattern. Here, we show that cholinergic signaling between the cloacal sensory/motor neurons and the posterior sex muscles sustains genital contact between the sexes. Simultaneously, via gap junctions, signaling from these muscles is transmitted to the spicule muscles, thus coupling repeated spicule thrusts with vulval contact. To transit from rhythmic to sustained muscle contraction during penetration, the SPC sensory-motor neurons integrate the signal of spicule's position in the vulva with inputs from the hook and cloacal sensilla. The UNC-103 K+ channel maintains a high excitability threshold in the circuit, so that sustained spicule muscle contraction is not stimulated by fewer inputs. We demonstrate that coordination of sensory inputs and motor outputs used to initiate, maintain, self-monitor, and complete an innate behavior is accomplished via the coupling of a few circuit components.


Zdroje

1. EmmonsSW

LiptonJ

2003 Genetic basis of male sexual behavior. J Neurobiol 54 93 110

2. LiuKS

SternbergPW

1995 Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14 79 89

3. de BonoM

MaricqAV

2005 Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci 28 451 501

4. LiptonJ

KleemannG

GhoshR

LintsR

EmmonsSW

2004 Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J Neurosci 24 7427 7434

5. 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

6. GruningerTR

GualbertoDG

LeBoeufB

GarciaLR

2006 Integration of male mating and feeding behaviors in Caenorhabditis elegans. J Neurosci 26 169 179

7. LeeK

PortmanDS

2007 Neural sex modifies the function of a C. elegans sensory circuit. Curr Biol 17 1858 1863

8. SenguptaP

SamuelAD

2009 Caenorhabditis elegans: a model system for systems neuroscience. Curr Opin Neurobiol 19 637 643

9. SokolowskiMB

2010 Social interactions in “simple” model systems. Neuron 65 780 794

10. BarrMM

GarciaLR

2006 Male mating behavior WormBook, ed The C elegans Research Community, WormBook, doi/101895/wormbook1781 http://wwwwormbookorg

11. SchaferWF

2006 Genetics of egg-laying in worms. Annu Rev Genet 40 487 509

12. BranickyR

HekimiS

2006 What keeps C. elegans regular: the genetics of defecation. Trends Genet 22 571 579

13. RankinCH

2006 Nematode behavior: the taste of success, the smell of danger! Curr Biol 16 R89 91

14. BargmannCI

2006 Chemosensation in C. elegans WormBook, ed The C elegans Research Community, WormBook, doi/101895/wormbook11231, http://wwwwormbookorg

15. GoodmanMB

2006 Mechanosensation WormBook, ed The C elegans Research Community, WormBook, http://wwwwormbookorg January 06

16. MoriI

SasakuraH

KuharaA

2007 Worm thermotaxis: a model system for analyzing thermosensation and neural plasticity. Curr Opin Neurobiol 17 712 719

17. ZhangM

ChungSH

Fang-YenC

CraigC

KerrRA

2008 A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior. Curr Biol 18 1445 1455

18. BarrMM

SternbergPW

1999 A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401 386 389

19. LiuT

KimK

LiC

BarrM

2007 FMRFamide-like neuropeptides and mechanosensory touch receptor neurons regulate male sexual turning behavior in Caenorhabditis elegans. J Neurosci 27 7174 7182

20. 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

21. WhittakerA

SternbergP

2009 Coordination of opposing sex-specific and core muscle groups regulates male tail posture during Caenorhabditis elegans male mating behavior. BMC Biol 7 33

22. GarciaLR

MehtaP

SternbergPW

2001 Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 107 777 788

23. KleemannGA

BasoloAL

2007 Facultative decrease in mating resistance in hermaphroditic Caenorhabditis elegans with self-sperm depletion. Animal Behaviour 74 1337 1347

24. GarciaLR

LeBoeufB

KooP

2007 Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes. Genetics 175 1761 1771

25. SulstonJE

AlbertsonDG

ThomsonJN

1980 The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev Biol 78 542 576

26. 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

27. FlemingJT

SquireMD

BarnesTM

TornoeC

MatsudaK

1997 Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci 17 5843 5857

28. RayesD

FlaminiM

HernandoG

BouzatC

2007 Activation of single nicotinic receptor channels from Caenorhabditis elegans muscle. Mol Pharmacol 71 1407 1415

29. RichmondJE

JorgensenEM

1999 One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat Neurosci 2 791 797

30. BallivetM

AlliodC

BertrandS

BertrandD

1996 Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. J Mol Biol 258 261 269

31. LewisJA

WuCH

BergH

LevineJH

1980 The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95 905 928

32. KimJ

PooleDS

WaggonerLE

KempfA

RamirezDS

2001 Genes affecting the activity of nicotinic receptors involved in Caenorhabditis elegans egg-laying behavior. Genetics 157 1599 1610

33. LewisJA

WuCH

LevineJH

BergH

1980 Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience 5 967 989

34. LeBoeufB

GruningerTR

GarciaLR

2007 Food deprivation attenuates seizures through CaMKII and EAG K+ channels. PLoS Genet 3 e156 doi:10.1371/journal.pgen.0030156

35. TouroutineD

FoxRM

Von StetinaSE

BurdinaA

MillerDM3rd

2005 acr-16 encodes an essential subunit of the levamisole-resistant nicotinic receptor at the Caenorhabditis elegans neuromuscular junction. J Biol Chem 280 27013 27021

36. JospinM

QiYB

StawickiTM

BoulinT

SchuskeKR

2009 A neuronal acetylcholine receptor regulates the balance of muscle excitation and inhibition in Caenorhabditis elegans. PLoS Biol 7 e1000265 doi:10.1371/journal.pbio.1000265

37. LintsR

HallDH

2009 Male muscle system, male-specific muscles. In WormAtlas doi:103908/wormatlas25

38. GowerNJ

WalkerDS

BaylisHA

2005 Inositol 1,4,5-trisphosphate signaling regulates mating behavior in Caenorhabditis elegans males. Mol Biol Cell 16 3978 3986

39. BennettMV

ZukinRS

2004 Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41 495 511

40. BennettMV

BarrioLC

BargielloTA

SprayDC

HertzbergE

1991 Gap junctions: new tools, new answers, new questions. Neuron 6 305 320

41. NagelG

BraunerM

LiewaldJF

AdeishviliN

BambergE

2005 Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15 2279 2284

42. NagelG

SzellasT

HuhnW

KateriyaS

AdeishviliN

2003 Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100 13940 13945

43. NakaiJ

OhkuraM

ImotoK

2001 A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19 137 141

44. ReinerDJ

WeinshenkerD

TianH

ThomasJH

NishiwakiK

2006 Behavioral genetics of caenorhabditis elegans unc-103-encoded erg-like K(+) channel. J Neurogenet 20 41 66

45. MatzMV

FradkovAF

LabasYA

SavitskyAP

ZaraiskyAG

1999 Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17 969 973

46. BairdGS

ZachariasDA

TsienRY

2000 Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97 11984 11989

47. ZhangF

PriggeM

BeyriereF

TsunodaSP

MattisJ

2008 Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat Neurosci 11 631 633

48. ReinerDJ

WeinshenkerD

ThomasJH

1995 Analysis of dominant mutations affecting muscle excitation in Caenorhabditis elegans. Genetics 141 961 976

49. PetersMA

TeramotoT

WhiteJQ

IwasakiK

JorgensenEM

2007 A calcium wave mediated by gap junctions coordinates a rhythmic behavior in C. elegans. Curr Biol 17 1601 1608

50. DavidsonJS

BaumgartenIM

1988 Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharmacol Exp Ther 246 1104 1107

51. SchneiderNL

StenglM

2006 Gap junctions between accessory medulla neurons appear to synchronize circadian clock cells of the cockroach Leucophaea maderae. J Neurophysiol 95 1996 2002

52. BaoL

SamuelsS

LocoveiS

MacagnoER

MullerKJ

2007 Innexins form two types of channels. FEBS Lett 581 5703 5708

53. RaizenDM

LeeRY

AveryL

1995 Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. Genetics 141 1365 1382

54. SattelleDB

CulettoE

GrausoM

RaymondV

FranksCJ

2002 Functional genomics of ionotropic acetylcholine receptors in Caenorhabditis elegans and Drosophila melanogaster. Novartis Found Symp 245 240 257; discussion 257-260, 261-244

55. AltunZF

ChenB

WangZW

HallDH

2009 High resolution map of Caenorhabditis elegans gap junction proteins. Dev Dyn 238 1936 1950

56. StarichT

SheehanM

JadrichJ

ShawJ

2001 Innexins in C. elegans. Cell Commun Adhes 8 311 314

57. SulstonJE

HorvitzHR

1977 Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56 110 156

58. BrennerS

1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

59. LiuQ

ChenB

GaierE

JoshiJ

WangZW

2006 Low conductance gap junctions mediate specific electrical coupling in body-wall muscle cells of Caenorhabditis elegans. J Biol Chem 281 7881 7889

60. 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

61. FranksCJ

MurrayC

OgdenD

O'ConnorV

Holden-DyeL

2009 A comparison of electrically evoked and channel rhodopsin-evoked postsynaptic potentials in the pharyngeal system of Caenorhabditis elegans. Invert Neurosci 9 43 56

62. BaierH

ScottEK

2009 Genetic and optical targeting of neural circuits and behavior—zebrafish in the spotlight. Curr Opin Neurobiol 19 553 560

63. GuoZV

HartAC

RamanathanS

2009 Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods 6 891 896

64. SchroederCE

WilsonDA

RadmanT

ScharfmanH

LakatosP

2010 Dynamics of Active Sensing and perceptual selection. Curr Opin Neurobiol 20 172 176

65. CroninCJ

MendelJE

MukhtarS

KimYM

StirblRC

2005 An automated system for measuring parameters of nematode sinusoidal movement. BMC Genet 6 5

66. ShadmehrR

SmithMA

KrakauerJW

2010 Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33 89 108

67. YuH

PretotR

BurglinT

SternbergP

2003 Distinct roles of transcription factors EGL-46 and DAF-19 in specifying the functionality of a polycystin-expressing sensory neuron necessary for C. elegans male vulva location behavior. Development 130 5217 5227

68. PedenE

BarrM

2005 The KLP-6 kinesin is required for male mating behaviors and polycystin localization in Caenorhabditis elegans. Curr Biol 15 394 404

69. JaureguiA

BarrM

2005 Functional characterization of the C. elegans nephrocystins NPHP-1 and NPHP-4 and their role in cilia and male sensory behaviors. Exp Cell Res 305 333 342

70. BaeY-K

Lyman-GingerichJ

BarrM

KnobelK

2008 Identification of genes involved in the ciliary trafficking of C. elegans PKD-2. Developmental Dynamics 237 2021 2029

71. WhiteJG

SouthgateE

ThomsonJN

BrennerS

1986 The Structure of the Nervous System of the Nematode Caenorhabditis elegans. Phil Trans Royal Soc London Series B, Biol Scien 314 1 340

72. MacoskoEZ

PokalaN

FeinbergEH

ChalasaniSH

ButcherRA

2009 A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458 1171 1175

73. ChenB

LiuQ

GeQ

XieJ

WangZW

2007 UNC-1 regulates gap junctions important to locomotion in C. elegans. Curr Biol 17 1334 1339

74. WagenaarDA

HamiltonMS

HuangT

KristanWB

FrenchKA

2010 A hormone-activated central pattern generator for courtship. Curr Biol 20 487 495

75. GrillnerS

WallenP

SaitohK

KozlovA

RobertsonB

2008 Neural bases of goal-directed locomotion in vertebrates—an overview. Brain Res Rev 57 2 12

76. GrillnerS

JessellTM

2009 Measured motion: searching for simplicity in spinal locomotor networks. Curr Opin Neurobiol 19 572 586

77. NisenbaumES

WilsonCJ

1995 Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15 4449 4463

78. KreitzerAC

MalenkaRC

2008 Striatal plasticity and basal ganglia circuit function. Neuron 60 543 554

79. MermelsteinPG

SongWJ

TkatchT

YanZ

SurmeierDJ

1998 Inwardly rectifying potassium (IRK) currents are correlated with IRK subunit expression in rat nucleus accumbens medium spiny neurons. J Neurosci 18 6650 6661

80. WilsonCJ

KawaguchiY

1996 The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16 2397 2410

81. GrillnerS

HellgrenJ

MenardA

SaitohK

WikstromMA

2005 Mechanisms for selection of basic motor programs—roles for the striatum and pallidum. Trends Neurosci 28 364 370

82. HodgkinJA

HorvitzHR

BrennerS

1979 Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91 67 94

83. ParkEC

HorvitzHR

1986 Mutations with dominant effects on the behavior and morphology of the nematode Caenorhabditis elegans. Genetics 113 821 852

84. SchnabelH

SchnabelR

1990 An Organ-Specific Differentiation Gene, pha-1, from Caenorhabditis elegans. Science 250 686 688

85. EdwardsS

CharlieN

MilfortM

BrownB

GravlinC

2008 A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans. PLoS Biol 6 e198 doi:10.1371/journal.pbio.0060198

86. BargmannCI

AveryL

1995 Laser killing of cells in Caenorhabditis elegans. Methods Cell Biol 48 225 250

87. Fang-YenC

WassermanS

SenguptaP

SamuelAD

2009 Agarose immobilization of C. elegans. Worm Breeder's Gazette 18 32

88. RualJF

CeronJ

KorethJ

HaoT

NicotAS

2004 Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14 2162 2168

89. 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


2011 Číslo 3
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