title: 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.
abstract: Many evolutionarily significant behaviors, such as mating, involve dynamic interactions with animate targets. This raises the question of what features of neural circuit design are essential to support these complex types of behavior. The Caenorhabditis elegans male uses 18 ray sensilla of the tail to coordinate mate apposition behavior, which facilitates a systematic search of the hermaphrodite surface for the vulva. Precisely how ray neuron types, A and B, robustly endow the male with a high degree of spatial and temporal precision is unknown. We show that the appositional postures that drive the search trajectory reflect the complex interplay of ray neuron type-induced motor outputs. Cell-type-specific ablations reveal that the A-neurons are required for all appositional postures. Their activity is instructive because the A-neurons can induce scanning- and turning-like appositional postures when artificially activated with channel rhodopsin (ChR2). B-neurons are essential only for initiation of the behavior in which they enhance male responsiveness to hermaphrodite contact. When artificially activated using ChR2, A- and B-neurons produce different tail ventral curl postures. However, when coactivated, A-neuron posture dominates, limiting B-neuron contributions to initiation or subsequent postures. Significantly, males lacking the majority of rays retain a high degree of postural control, indicating significant functional resilience in the system. Furthermore, eliminating a large number of male-specific ray neuron targets only partially attenuates tail posture control revealing that gender-common cells make an important contribution to the behavior. Thus, robustness may be a crucial feature of circuits underlying complex behaviors, such as mating, even in simple animals.
authors: Department of Biology, Texas A & M University, College Station, Texas 77843-3258, USA.
authors: Pamela K
authors: PK
authors: Koo
authors: Xuelin
authors: X
authors: Bian
authors: Amrita L
authors: AL
authors: Sherlekar
authors: Meredith R
authors: MR
authors: Bunkers
authors: Robyn
authors: R
authors: Lints
references: BMC Biol. 2009 Jun 22;7:33
references: 19545405
references: Curr Biol. 2001 Sep 4;11(17):1341-6
references: 11553327
references: J Neurosci. 1985 Apr;5(4):956-64
references: 3981252
references: Curr Biol. 2007 Nov 6;17(21):1858-63
references: 17964163
references: J Neurosci. 2007 Jul 4;27(27):7174-82
references: 17611271
references: J Comp Physiol A. 1999 Oct;185(4):373-8
references: 10555271
references: Dev Biol. 1977 Mar;56(1):110-56
references: 838129
references: Nat Rev Neurosci. 2007 Jul;8(7):510-21
references: 17585304
references: J Neurosci. 2007 Feb 7;27(6):1411-21
references: 17287516
references: Methods Cell Biol. 1995;48:451-82
references: 8531738
references: J Cell Biol. 2010 Jul 12;190(1):9-20
references: 20624897
references: Genetics. 1979 Jan;91(1):67-94
references: 17248881
references: Nature. 2007 Aug 30;448(7157):1009-14
references: 17676034
references: Neuron. 1991 Nov;7(5):729-42
references: 1660283
references: Genes Dev. 2010 Nov 1;24(21):2365-82
references: 21041406
references: Nat Rev Neurosci. 2010 Jan;11(1):18-29
references: 19953103
references: Genetics. 1998 Jan;148(1):187-200
references: 9475731
references: Genetics. 2010 Jul;185(3):883-96
references: 20421600
references: Methods Cell Biol. 1995;48:225-50
references: 8531727
references: Comp Biochem Physiol A Mol Integr Physiol. 2008 Aug;150(4):369-77
references: 18514002
references: Cell. 2008 Apr 18;133(2):354-63
references: 18423205
references: Development. 1994 Oct;120(10):3005-17
references: 7607088
references: Mol Biol Cell. 1998 Jun;9(6):1235-52
references: 9614171
references: Dev Biol. 1980 Aug;78(2):542-76
references: 7409314
references: Nature. 1995 Jan 5;373(6509):74-8
references: 7800042
references: J Neurosci. 1993 Dec;13(12):5407-17
references: 8254383
references: Neuron. 2010 Aug 12;67(3):381-91
references: 20696377
references: Development. 1999 Dec;126(24):5819-31
references: 10572056
references: Genes Dev. 2007 Dec 1;21(23):3181-94
references: 18056428
references: Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):11002-7
references: 18667708
references: Curr Biol. 2006 Apr 4;16(7):649-59
references: 16581509
references: Cell. 1993 Jul 16;74(1):43-55
references: 8101475
references: Genetics. 2007 Apr;175(4):1761-71
references: 17277358
references: Nature. 2002 Dec 12;420(6916):669-73
references: 12478294
references: J Neurosci. 2004 Feb 4;24(5):1217-25
references: 14762140
references: Science. 2010 Oct 1;330(6000):55-60
references: 20813920
references: Science. 2000 Mar 24;287(5461):2229-34
references: 10744543
references: Science. 1998 Sep 11;281(5383):1686-90
references: 9733518
references: Dev Biol. 1981 Mar;82(2):358-70
references: 7227647
references: Genetics. 1974 May;77(1):71-94
references: 4366476
references: Curr Biol. 2007 Nov 6;17(21):1847-57
references: 17964166
references: Neuron. 1995 Jan;14(1):79-89
references: 7826644
references: Dev Biol. 2004 May 1;269(1):137-51
references: 15081363
references: Nat Methods. 2009 Dec;6(12):891-6
references: 19898486
references: Science. 2003 Jul 4;301(5629):96-9
references: 12805553
references: Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2283-8
references: 17283333
references: J Neurosci. 2001 Dec 1;21(23):9265-72
references: 11717360
references: J Comp Neurol. 1975 Sep 15;163(2):215-26
references: 240872
references: Nature. 2000 Feb 3;403(6769):560-4
references: 10676966
references: Cell. 1993 Jul 16;74(1):29-42
references: 8101474
references: Dis Model Mech. 2010 Jul-Aug;3(7-8):441-50
references: 20223935
references: Genetics. 2009 Jan;181(1):153-63
references: 19001289
references: BMC Biol. 2006 Aug 15;4:26
references: 16911797
references: Curr Biol. 2008 Dec 9;18(23):1865-71
references: 19062284
references: Genes Dev. 1993 Sep;7(9):1714-24
references: 8103754
references: Cell. 1986 Aug 1;46(3):477-87
references: 3731276
references: Annu Rev Neurosci. 2005;28:451-501
references: 16022603
references: Exp Cell Res. 2008 Feb 15;314(4):825-33
references: 18037411
references: Nature. 2006 Mar 30;440(7084):684-7
references: 16572173
references: Nature. 1999 Sep 23;401(6751):386-9
references: 10517638
references: Curr Biol. 2005 Dec 20;15(24):2279-84
references: 16360690