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Sensory Neurons Arouse C. elegans Locomotion via Both Glutamate and Neuropeptide Release.

Choi S, Taylor KP, Chatzigeorgiou M, Hu Z, Schafer WR, Kaplan JM - PLoS Genet. (2015)

Bottom Line: Lethargus and adult locomotion quiescence is dramatically reduced in mutants lacking the neuropeptide receptor NPR-1.These sensory neurons accelerate locomotion via both neuropeptide and glutamate release.Our results suggest that a broad network of sensory neurons dictates transitions between aroused and quiescent behavioral states.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts, United States of America; Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America; Biological and Biomedical Sciences program, Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT
C. elegans undergoes periods of behavioral quiescence during larval molts (termed lethargus) and as adults. Little is known about the circuit mechanisms that establish these quiescent states. Lethargus and adult locomotion quiescence is dramatically reduced in mutants lacking the neuropeptide receptor NPR-1. Here, we show that the aroused locomotion of npr-1 mutants results from the exaggerated activity in multiple classes of sensory neurons, including nociceptive (ASH), touch sensitive (ALM and PLM), and stretch sensing (DVA) neurons. These sensory neurons accelerate locomotion via both neuropeptide and glutamate release. The relative contribution of these sensory neurons to arousal differs between larval molts and adults. Our results suggest that a broad network of sensory neurons dictates transitions between aroused and quiescent behavioral states.

No MeSH data available.


Related in: MedlinePlus

Inactivating PDF signaling does not prevent aroused locomotion in npr-1 adults.(A-B) The npr-1 aldicarb hypersensitivity was decreased but not abolished by mutations inactivating PDF-1 or PDFR-1. The percentage of animals paralyzed on 1 mM aldicarb at 80 min were plotted for the indicated genotypes. The number of trials is indicated for each genotype. Full time courses of aldicarb-induced paralysis are shown in S2D and S2E Fig. (C) Locomotion behavior of single adult worms was analyzed for the indicated genotypes. The npr-1 adult locomotion defect was not blocked by mutations inactivating PDF-1 or PDFR-1. (D-F) mEPSCs were recorded from body wall muscles of adult worms for the indicated genotypes. Representative traces of mEPSCs (D) and summary data are shown (E-F). The npr-1 cholinergic transmission defect was not suppressed by mutations inactivating PDFR-1. The number of animals analyzed is indicated for each genotype. Error bars indicate SEM. Values that differ significantly are indicated (*, p<0.05;**, p<0.01;***, p <0.001; ns, not significant).
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pgen.1005359.g002: Inactivating PDF signaling does not prevent aroused locomotion in npr-1 adults.(A-B) The npr-1 aldicarb hypersensitivity was decreased but not abolished by mutations inactivating PDF-1 or PDFR-1. The percentage of animals paralyzed on 1 mM aldicarb at 80 min were plotted for the indicated genotypes. The number of trials is indicated for each genotype. Full time courses of aldicarb-induced paralysis are shown in S2D and S2E Fig. (C) Locomotion behavior of single adult worms was analyzed for the indicated genotypes. The npr-1 adult locomotion defect was not blocked by mutations inactivating PDF-1 or PDFR-1. (D-F) mEPSCs were recorded from body wall muscles of adult worms for the indicated genotypes. Representative traces of mEPSCs (D) and summary data are shown (E-F). The npr-1 cholinergic transmission defect was not suppressed by mutations inactivating PDFR-1. The number of animals analyzed is indicated for each genotype. Error bars indicate SEM. Values that differ significantly are indicated (*, p<0.05;**, p<0.01;***, p <0.001; ns, not significant).

Mentions: We previously showed that the lethargus quiescence defects exhibited by npr-1 mutants are caused by increased secretion of Pigment dispersing factor (PDF-1) by cells in the RMG circuit [11]. Because PDF-1 secretion is also increased in npr-1 adults [11], we tested the idea that the hyperactive adult locomotion of npr-1 mutants is also caused by increased PDF signaling. Contrary to this idea, we found that pdf-1 and pdfr-1 (PDF Receptor-1) mutations reduced but did not eliminate the aldicarb hypersensitivity (Fig 2A and 2B and S2D and S2E Fig), the accelerated locomotion (Fig 2C), and increased mEPSC rate (Fig 2D and 2E) defects of npr-1 adults. Collectively, these results suggest that additional excitatory outputs from the RMG circuit (i.e. beyond PDF-1) must contribute to the aroused locomotion of npr-1 adults.


Sensory Neurons Arouse C. elegans Locomotion via Both Glutamate and Neuropeptide Release.

Choi S, Taylor KP, Chatzigeorgiou M, Hu Z, Schafer WR, Kaplan JM - PLoS Genet. (2015)

Inactivating PDF signaling does not prevent aroused locomotion in npr-1 adults.(A-B) The npr-1 aldicarb hypersensitivity was decreased but not abolished by mutations inactivating PDF-1 or PDFR-1. The percentage of animals paralyzed on 1 mM aldicarb at 80 min were plotted for the indicated genotypes. The number of trials is indicated for each genotype. Full time courses of aldicarb-induced paralysis are shown in S2D and S2E Fig. (C) Locomotion behavior of single adult worms was analyzed for the indicated genotypes. The npr-1 adult locomotion defect was not blocked by mutations inactivating PDF-1 or PDFR-1. (D-F) mEPSCs were recorded from body wall muscles of adult worms for the indicated genotypes. Representative traces of mEPSCs (D) and summary data are shown (E-F). The npr-1 cholinergic transmission defect was not suppressed by mutations inactivating PDFR-1. The number of animals analyzed is indicated for each genotype. Error bars indicate SEM. Values that differ significantly are indicated (*, p<0.05;**, p<0.01;***, p <0.001; ns, not significant).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4495980&req=5

pgen.1005359.g002: Inactivating PDF signaling does not prevent aroused locomotion in npr-1 adults.(A-B) The npr-1 aldicarb hypersensitivity was decreased but not abolished by mutations inactivating PDF-1 or PDFR-1. The percentage of animals paralyzed on 1 mM aldicarb at 80 min were plotted for the indicated genotypes. The number of trials is indicated for each genotype. Full time courses of aldicarb-induced paralysis are shown in S2D and S2E Fig. (C) Locomotion behavior of single adult worms was analyzed for the indicated genotypes. The npr-1 adult locomotion defect was not blocked by mutations inactivating PDF-1 or PDFR-1. (D-F) mEPSCs were recorded from body wall muscles of adult worms for the indicated genotypes. Representative traces of mEPSCs (D) and summary data are shown (E-F). The npr-1 cholinergic transmission defect was not suppressed by mutations inactivating PDFR-1. The number of animals analyzed is indicated for each genotype. Error bars indicate SEM. Values that differ significantly are indicated (*, p<0.05;**, p<0.01;***, p <0.001; ns, not significant).
Mentions: We previously showed that the lethargus quiescence defects exhibited by npr-1 mutants are caused by increased secretion of Pigment dispersing factor (PDF-1) by cells in the RMG circuit [11]. Because PDF-1 secretion is also increased in npr-1 adults [11], we tested the idea that the hyperactive adult locomotion of npr-1 mutants is also caused by increased PDF signaling. Contrary to this idea, we found that pdf-1 and pdfr-1 (PDF Receptor-1) mutations reduced but did not eliminate the aldicarb hypersensitivity (Fig 2A and 2B and S2D and S2E Fig), the accelerated locomotion (Fig 2C), and increased mEPSC rate (Fig 2D and 2E) defects of npr-1 adults. Collectively, these results suggest that additional excitatory outputs from the RMG circuit (i.e. beyond PDF-1) must contribute to the aroused locomotion of npr-1 adults.

Bottom Line: Lethargus and adult locomotion quiescence is dramatically reduced in mutants lacking the neuropeptide receptor NPR-1.These sensory neurons accelerate locomotion via both neuropeptide and glutamate release.Our results suggest that a broad network of sensory neurons dictates transitions between aroused and quiescent behavioral states.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts, United States of America; Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States of America; Biological and Biomedical Sciences program, Harvard Medical School, Boston, Massachusetts, United States of America.

ABSTRACT
C. elegans undergoes periods of behavioral quiescence during larval molts (termed lethargus) and as adults. Little is known about the circuit mechanisms that establish these quiescent states. Lethargus and adult locomotion quiescence is dramatically reduced in mutants lacking the neuropeptide receptor NPR-1. Here, we show that the aroused locomotion of npr-1 mutants results from the exaggerated activity in multiple classes of sensory neurons, including nociceptive (ASH), touch sensitive (ALM and PLM), and stretch sensing (DVA) neurons. These sensory neurons accelerate locomotion via both neuropeptide and glutamate release. The relative contribution of these sensory neurons to arousal differs between larval molts and adults. Our results suggest that a broad network of sensory neurons dictates transitions between aroused and quiescent behavioral states.

No MeSH data available.


Related in: MedlinePlus