A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans - PubMed (original) (raw)

. 2009 Apr 30;458(7242):1171-5.

doi: 10.1038/nature07886. Epub 2009 Apr 6.

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A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans

Evan Z Macosko et al. Nature. 2009.

Abstract

Innate social behaviours emerge from neuronal circuits that interpret sensory information on the basis of an individual's own genotype, sex and experience. The regulated aggregation behaviour of the nematode Caenorhabditis elegans, a simple animal with only 302 neurons, is an attractive system to analyse these circuits. Wild social strains of C. elegans aggregate in the presence of specific sensory cues, but solitary strains do not. Here we identify the RMG inter/motor neuron as the hub of a regulated circuit that controls aggregation and related behaviours. RMG is the central site of action of the neuropeptide receptor gene npr-1, which distinguishes solitary strains (high npr-1 activity) from wild social strains (low npr-1 activity); high RMG activity is essential for all aspects of social behaviour. Anatomical gap junctions connect RMG to several classes of sensory neurons known to promote aggregation, and to ASK sensory neurons, which are implicated in male attraction to hermaphrodite pheromones. We find that ASK neurons respond directly to pheromones, and that high RMG activity enhances ASK responses in social strains, causing hermaphrodite attraction to pheromones at concentrations that repel solitary hermaphrodites. The coordination of social behaviours by RMG suggests an anatomical hub-and-spoke model for sensory integration in aggregation, and points to functions for related circuit motifs in the C. elegans wiring diagram.

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Figures

Figure 1

Figure 1. Selective expression of NPR-1 suppresses aggregation and related behaviors in npr-1 mutants

a, Solitary behavior of 150 wild type N2 animals (left) and aggregation behavior of 150 npr-1(ad609) animals (right). b, Behavioral phenotypes of npr-1(ad609) animals expressing an npr-1 cDNA under a pan-neuronal promoter (tag-168), its endogenous promoter (npr-1), URX promoters (gcy-32 and flp-8) and RMG promoters (ncs-1 and flp-21). For all figures, full promoter expression patterns are in Supplementary Table 1. Error bars indicate standard deviation (s.d.). Asterisk, different from npr-1(ad609) (P < 0.01, Bonferroni test).

Figure 2

Figure 2. Inhibition of RMG by NPR-1 suppresses social behavior

a, Top, intersectional Cre/Lox strategy to express npr-1 specifically in RMG. Bottom, L4 larva expressing ncs-1::nCre and flp-21::LoxStopLox::GFP. b, Aggregation and related behaviors of npr-1(ad609) animals carrying ncs-1::nCre and/or flp-21::LoxStopLox::npr-1 transgenes. Asterisk, different from npr-1(ad609) (P < 0.01, Student's t-test). c, Mock-ablated or RMG-ablated npr-1(ad609) animals (mock-ablated: 97.1% bordering, 40% aggregating. RMG-ablated: 17% bordering, 0% aggregating. χ2 = 43.05, P < 0.001). d, Locomotion speed of WT and npr-1(ad609) animals, mock-ablated or RMG ablated. Asterisk, different from mock-ablated npr-1(ad609) (P < 0.01, Student's t-test). Error bars indicate s.d.

Figure 3

Figure 3. ASK and ASJ sensory neurons promote aggregation

a, Circuit diagram of neurons with gap junctions to RMG. RMG may also form gap junctions with RMF. b, Rescue of aggregation and related behaviors in tax-4(p678);npr-1(ad609) animals expressing a tax-4 cDNA. Asterisk, different from tax-4;npr-1. c, Aggregation and related behaviors of npr-1(ad069) animals expressing tetanus toxin light chain (TeTx). Statistics: different from (1)npr-1(ad609) (2)npr-1(ad609) and overlapping single-transgene strains. d, Aggregation and related behaviors of wild-type animals expressing gain-of-function protein kinase C (pkc-1(gf)). Statistics: different from (1)WT (2)WT and overlapping single-transgene strains. In b-d, P<0.01, Bonferroni test. Error bars indicate s.d.

Figure 4

Figure 4. Behavioral and neuronal responses to pheromones

a, Diagram of pheromone chemotaxis assay. b, Ascaroside chemotaxis. Asterisk, different from npr-1(ad609). c, ASK expression of tax-4 restores pheromone attraction to tax-4;npr-1. Asterisk, different from tax-4;npr-1. d, TeTx expression in RMG or ASJ and ASK eliminates pheromone attraction in npr-1(ad609). Asterisk, different from npr-1(ad609). In b-d, P<0.01, Bonferroni test. e, Ascaroside (100 nM) decreases G-CaMP calcium signals in ASK (n=17 animals each). f, Average ASK fluorescence change to first ascaroside addition (ON) and removal (OFF). Asterisks, different from wild-type (P < 0.01, t-test). g, Ascaroside (1 μM) induces G-CaMP calcium signals in AIA interneurons of npr-1(ad609); for ablations, n≥10 animals; mock-ablated, n=16. In e and g, dark shading indicates presence of ascarosides, light shading indicates standard error of the mean (s.e.m). h, Average AIA fluorescence change in 5s after ascaroside addition. Asterisk, different from mock-ablated (P<0.01, Bonferroni test). In b-d, f and h, error bars indicate s.e.m.

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