Neurexin controls plasticity of a mature, sexually dimorphic neuron

Abstract

During development and adulthood, brain plasticity is evident at several levels, from synaptic structure and function to the outgrowth of dendrites and axons. Whether and how sex impinges on neuronal plasticity is poorly understood. Here we show that the sex-shared GABA (γ-aminobutyric acid)-releasing DVB neuron in Caenorhabditis elegans displays experience-dependent and sexually dimorphic morphological plasticity, characterized by the stochastic and dynamic addition of multiple neurites in adult males. These added neurites enable synaptic rewiring of the DVB neuron and instruct a functional switch of the neuron that directly modifies a step of male mating behaviour. Both DVB neuron function and male mating behaviour can be altered by experience and by manipulation of postsynaptic activity. The outgrowth of DVB neurites is promoted by presynaptic neurexin and antagonized by postsynaptic neuroligin, revealing a non-conventional activity and mode of interaction of these conserved, human-disease-relevant factors.

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Figure 1: Progressive neurite outgrowth of the GABAergic DVB neuron in adult males.
Figure 2: DVB neuron undergoes a functional switch in adulthood resulting in dynamic behavioural output.
Figure 3: DVB neurite outgrowth is experience-dependent, can be driven by circuit activity, and affects behaviour.
Figure 4: Neuroligin and neurexin influence DVB neurite outgrowth and spicule protraction behaviour.

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Acknowledgements

We thank Q. Chen for generating transgenic strains and M. Gendrel for DVB promoter and reporter lines; P. Sengupta, T. G. Drivas, M. Oren-Suissa, and members of the Hobert laboratory for comments on the manuscript; L. R. Garcia and K. Shen for worm strains; and M. VanHoven and D. Colon-Ramos for plasmids. This work was supported by NIH grants from NINDS (M.P.H.:F32NS086285; O.H.:2R37NS039996). O.H. is a Howard Hughes Medical Institute investigator. Some strains were provided by the CGC, funded by NIH Office of Research Infrastructure Programs (P40 OD010440).

Author information

M.P.H. and O.H. designed the experiments and wrote the manuscript. M.P.H. performed the experiments.

Correspondence to Michael P. Hart.

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Extended data figures and tables

Extended Data Figure 1 Progressive neurite outgrowth in DVB in adulthood.

ac, DVB neuron visualized with lim-6int4::gfp at days 1, 3, and 5 in adult males (a) and quantification of total neurite length (b) and number of neurite junctions (c) (dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05)). d, DVB neurite outgrowth visualized with flp-10::gfp in males at days 1, 3, and 5 of adulthood (n > 10, scale bars, 10 μm). e, Tracing reconstruction of male DVB from electron micrograph sections compiled by http://wormwiring.org showing DVB neurites. f, Inset of DVB neurites showing presynaptic specializations identified in electron micrograph sections shown in pink. g, h, Electron micrograph section showing DVB pseudo-coloured yellow with presynaptic specialization indicated with red x with SPCR (Image Right1200, Section 14871) (g) and spicule sheath (Image N2YDRG1175, Section 14816) (h), shown in white in inset panel. Scale bars, 1 μm.

Extended Data Figure 2 DVB neurite outgrowth in adult male C. elegans is stochastic and other neurons in the male tail do not show progressive neurite outgrowth in adulthood.

a, b, DVB neurites at day 5 visualized with lim-6int4::wCherry (a) or lim-6int4::gfp (b) (n > 10 for each). DVB posterior neurites were traced through confocal stacks using Simple Neurite Tracer4 plugin. c, DVA neuron visualized with ser-2(prom-2)::gfp (n = 5) (red dashed line indicates axon of relevant neuron). d, DVC neuron visualized with inx-18p::gfp (n = 5). e, CP6 neuron visualized with flp-13::gfp (cell soma not shown) (n = 5). f, Ray neurons visualized with dat-1::gfp (ventral view) (n = 5). g, h, PVT neuron visualized with srz-102p::gfp (n = 5) (g) and srg-4p::gfp (n = 5) (h) at day 1 and day 5. Axons of indicated neurons highlighted by red dashed lines. Scale bars, 10 μm.

Extended Data Figure 3 DVB inhibits expulsion-associated spicule protraction at day 3.

Laser ablation of DVB and channelrhodopsin expression in DVB and spicule protraction circuit. a, Confocal images of male worm with lim-6int4::wCherry and lim-6int4::HisCl1::gfp at day 3. b, Quantification of the percentage of expulsion steps with spicule protraction for day 1 control, day 3 control, day 3 control + histamine, and day 3 lim-6int4::HisCl1::gfp + histamine males. c, Time between consecutive expulsion steps for day 1 control, day 3 control, day 3 control + histamine, and day 3 lim-6int4::HisCl1::gfp + histamine males (+ histamine is on 10 mM histamine plates; dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05)). d, Confocal images of male worms with or without laser ablation of DVB at day 1 or 2, visualized with lim-6int4::gfp. e, Confocal images of DVB (lim-6int4::wCherry) expressing channelrhodopsin at day 1 and 5, Ex[lim-6int4::ChR2::yfp]. f, Confocal images of DVB (lim-6int4::wCherry) and spicule circuit expressing channelrhodopsin at day 1 and 5, Ex[gar-3b::ChR2::yfp]. n > 10 for df. Scale bars, 10 μm.

Extended Data Figure 4 DVB neurite outgrowth in unc-49, pkd-2 and unc-97 mutant males.

flp-13p::gfp labels CP6 and spicule retractor muscles. ac, Confocal images (a) and quantification of total neurite outgrowth (b) and number of neurite junctions (c) in control and unc-49(e407) males at days 3 and 5. d, Time to spicule protraction on aldicarb at day 5 for control and unc-49(e407) males. eg, Confocal images (e) and quantification of total neurite outgrowth (f) and number of neurite junctions (g) in control, pkd-2(pt8), and unc-97(su110) males at day 3. h, Confocal images of male worms with lim-6int4::wCherry, flp-10p::gfp, and differential interference contrast at day 1 in ventral and lateral views. Inset showing DVB and CP6 axons, with schematic of axons demonstrating lack of contact (red is DVB axon, green is CP6 axon, blue dashed lines are spicule retractor muscles). Asterisks in flp-13::gfp panel mark spicule retractor muscles. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

Extended Data Figure 5 Day 1 male mating defects involving spicule coordination, spicule circuit activation in unc-25, unc-97, and nrx-1 mutant males, and spicule neuron or muscle activation induces DVB neurite outgrowth.

a, Per cent average mating success (sperm transfer) for day 1 and 3 males during 5-min timed mating assays with 15 unc-31(e928) hermaphrodites (n is number of worms, data points represent average percentage for each replicate of multiple males). b, Quantification of attempts at spicule prodding during 5-min timed mating assay for day 1 and 3 males. c, Ratio of protraction:prodding attempts during 5-min timed mating assay for males at days 1 and 3. df, Confocal images of lim-6int4::wCherry (d), total neurite length (e), and number or neurite junctions (f) of unc-25(e156), unc-25(e156);Ex[gar-3b::ChR2::yfp], unc-97(su110), unc-97(su110);Ex[gar-3b::ChR2::yfp], nrx-1(wy778), and nrx-1(wy778);Ex[gar-3b::ChR2::yfp] males following activation at day 1 (488-nm light for 3 × 15 s every 45 min for 4.5 h). gi, Confocal images (g) and quantification of total neurite outgrowth (h) and number of neurite junctions (i) in control, Ex[unc-103E::ChR2::yfp], and Ex[unc-103F4::ChR2::yfp] worms after activation at day 1 with retinal (488-nm light for 3 × 5 s every 45 min for 4.5 h). j, k, Quantification of total neurite outgrowth (j) and number of neurite junctions (k) at day 1 in control, Ex[lim-6int4::ChR2::yfp] (DVB), Ex[unc-103E::ChR2::yfp] (neuron-specific), and Ex[unc-103F4::ChR2::yfp] (muscle-specific) males after activation but in the absence of retinal. l, Time to protraction of control and Ex[lim-6int4::ChR2::yfp] males after day 1 activation in the absence of retinal. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

Extended Data Figure 6 Exposure to exogenous GABA or silencing of spicule protraction circuit activity overnight reduces DVB neurites on day 5.

ac, Confocal images of lim-6int4::wCherry (a), total neurite length (b), and number or neurite junctions (c) of males exposed overnight to 30 mM GABA at days 3 and 5. df, Confocal images of lim-6int4::wCherry (d), total neurite length (e), and number of neurite junctions (f) at day 5 of control worms with or without overnight 10 mM histamine, and gar-3b::HisCl1::gfp worms with or without overnight 10 mM histamine. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

Extended Data Figure 7 NLG-1 expression in multiple male sex muscles rescues nlg-1 mutant DVB neurite phenotype.

Silencing spicule circuit or exposure to exogenous GABA does not reduce DVB neurites in nlg-1 mutant males. ac, Confocal images of DVB (lim-6int4::wCherry) (a), and quantification of total neurite outgrowth (b) and number of neurite junctions (c) in control, nlg-1(ok259), nlg-1(ok259);nlg-1p::nlg-1::gfp, and nlg-1p::nlg-1::gfp day 3 males. d, e, Quantification of total neurite outgrowth (d) and number of neurite junctions (e) in control or nlg-1(ok259) mutant males with or without tissue-specific NLG-1 expression. Expression patterns for rescue promoters: lim-6int4 in DVB; gar-3b in SPC and spicule protractor muscles; unc-103F in SPC, PCA, PCB and other neurons; unc-103E in male sex muscles; flp-13 in spicule retractor muscles and CP6. fh, Confocal images (f) of lim-6int4::wCherry and Ex[gar-3b::HisCl1::gfp] in day 5 male worms, with total neurite length (g) and number of neurite junctions (h) of nlg-1(ok259) worms with or without 10 mM histamine overnight, nlg-1(ok259); gar-3b::HisCl1::gfp worms with or without 10 mM histamine overnight, and nlg-1(ok259) worms with 30 mM GABA overnight. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

Extended Data Figure 8 NLG-1 expression decreases from day 1 to day 3.

a, Confocal images of nlg-1p::nlg-1::gfp in males at days 1, 3, and 5. Example regions of interest for measurements taken from single planes: blue, dorsal spicule muscles; red, pre-anal ganglion; magenta, DVB. b, c, Quantification of fluorescence intensity of nlg-1p::nlg-1::gfp in males at days 1, 3, and 5 reported as a ratio of mean fluorescence in dorsal spicule muscles (b) or pre-anal ganglion (c) normalized to background of DVB, which has little-to-undetectable expression. Dorsal spicule muscles refer to the gubernacular retractor, gubernacular erector, anterior oblique, and anal depressor. d, Confocal images of nlg-1p::nlg-1::gfp in day 3 males as follows: control, nlg-1(ok259), nlg-1(ok259) with overnight GABA exposure, nlg-1(ok259) with 3-day GABA exposure, and nrx-1(wy778). e, f, Quantification of fluorescence intensity of nlg-1p::nlg-1::gfp in day 1 and 3 male worms as follows: control, nlg-1(ok259), nrx-1(wy778), day 3 nlg-1(ok259) with overnight GABA exposure, and nlg-1(ok259) with 3-day GABA exposure, as a ratio of mean fluorescence in dorsal spicule muscles (e) or pre-anal ganglion (f) normalized to background of DVB. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

Extended Data Figure 9 NRX-1 long isoform functions in DVB to control DVB neurite outgrowth and NRX-1 expression in DVB controls neurite outgrowth of nlg-1 mutants.

a, Genetic loci of nrx-1 showing long and short isoforms, PDZ binding motif, and locations of point mutation gk246237 and deletions ok1649 and wy778. b, c, Quantification of total neurite length (b) and number of neurite junctions (c) in controls and long-isoform-specific mutants nrx-1(ok1649) and nrx-1(gk246237) at day 3. d, e, Quantification of total neurite outgrowth (d) and number of neurite junctions (e) at day 3 in control, Ex[lim-6int4::birA::nrx-1LONG], nrx-1(wy778), nrx-1(wy778);Ex[lim-6int4::birA::nrx-1LONG], nrx-1(wy778);Ex[lim-6int4::birA::nrx-1SHORT], and nrx-1(wy778);Ex[lim-6int4::birA::nrx-1noPDZ] worms. f, Time to spicule protraction at day 3 in control, nrx-1(wy778), nrx-1(wy778);Ex[lim-6int4::birA::nrx-1LONG], and Ex[lim-6int4::birA::nrx-1LONG] worms. gi, Confocal images of lim-6int4::wCherry expression (g) and quantification of total neurite length (h) and number of neurite junctions (i) of day 3 nlg-1(ok259), nlg-1(ok259);Ex[lim-6int4::birA::nrx-1LONG], nrx-1(wy778), nrx-1(wy778);nlg-1(ok259), and nrx-1(wy778);nlg-1(ok259);Ex[lim-6int4::birA::nrx-1LONG] males. j, Confocal images of lim-6int4::wCherry and Ex[lim-6int4::gfp::nrx-1LONG] in control, nrx-1(wy778), and nlg-1(ok259) males at day 1 and 3. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05) scale bars, 10 μm.

Extended Data Figure 10 DVB in hermaphrodites does not show neurite branching upon gar-3b::ChR2::yfp activation or NRX-1 or NLG-1 manipulation.

a, Confocal images of lim-6int4::wCherry and Ex[gar-3b::ChR2::yfp] expression in day 1 hermaphrodites showing DVB axon projection after activation with retinal (488-nm light for 3 × 15 s every 45 min for 4.5 h). b, Confocal images of lim-6int4::wCherry or lim-6int4::gfp in control, nrx-1(wy778), nlg-1(ok259), and Ex[lim-6int4::gfp::nrx-1LONG] hermaphrodites at day 3. c, Quantification of the percentage of hermaphrodites with DVB axon abnormalities or neurites (in almost all cases, a single neurite off the axon just posterior to the pre-anal ganglion) in day 1 control and Ex[gar-3b::ChR2::yfp] with activation, day 3 control, nrx-1(wy778), nlg-1(ok259), and Ex[lim-6int4::gfp::nrx-1LONG] worms. n shows number of worms, data points represent average percentage for each replicate of multiple hermaphrodites. Dot represents one worm; magenta bar, median; boxes, quartiles; one-way ANOVA and post-hoc Tukey HSD, P values shown above plots, bold shows significance (P < 0.05), scale bars, 10 μm.

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Life Sciences Reporting Summary (PDF 72 kb)

Supplementary Table 1

This file contains the strain list. (XLSX 35 kb)

Spicule Protraction

A male expressing Ex[lim-6int4::ChR2::yfp] demonstrating spicule muscle contraction upon blue light activation (blue dot indicates 488 nm light exposure). (MP4 4036 kb)

Spicule Protraction

A male expressing Ex[gar-3b::ChR2::yfp] demonstrating spicule protraction upon blue light activation (blue dot indicates 488 nm light exposure). (MP4 10475 kb)

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Hart, M., Hobert, O. Neurexin controls plasticity of a mature, sexually dimorphic neuron. Nature 553, 165–170 (2018) doi:10.1038/nature25192

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