Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition
Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogen...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2016-11-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/21126 |
_version_ | 1811253336801804288 |
---|---|
author | Kevin M Collins Addys Bode Robert W Fernandez Jessica E Tanis Jacob C Brewer Matthew S Creamer Michael R Koelle |
author_facet | Kevin M Collins Addys Bode Robert W Fernandez Jessica E Tanis Jacob C Brewer Matthew S Creamer Michael R Koelle |
author_sort | Kevin M Collins |
collection | DOAJ |
description | Like many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states. |
first_indexed | 2024-04-12T16:49:21Z |
format | Article |
id | doaj.art-ebe22fcff2cc4706943a6e372af82db4 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T16:49:21Z |
publishDate | 2016-11-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
spelling | doaj.art-ebe22fcff2cc4706943a6e372af82db42022-12-22T03:24:27ZengeLife Sciences Publications LtdeLife2050-084X2016-11-01510.7554/eLife.21126Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibitionKevin M Collins0https://orcid.org/0000-0001-9930-0924Addys Bode1Robert W Fernandez2Jessica E Tanis3Jacob C Brewer4https://orcid.org/0000-0003-2780-2874Matthew S Creamer5Michael R Koelle6https://orcid.org/0000-0001-9486-8481Department of Biology, University of Miami, Coral Gables, United States; Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United StatesDepartment of Biology, University of Miami, Coral Gables, United StatesDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, United StatesDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, United StatesDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, United StatesInterdepartmental Neuroscience Program, Yale University, New Haven, United StatesDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States; Interdepartmental Neuroscience Program, Yale University, New Haven, United StatesLike many behaviors, Caenorhabditis elegans egg laying alternates between inactive and active states. To understand how the underlying neural circuit turns the behavior on and off, we optically recorded circuit activity in behaving animals while manipulating circuit function using mutations, optogenetics, and drugs. In the active state, the circuit shows rhythmic activity phased with the body bends of locomotion. The serotonergic HSN command neurons initiate the active state, but accumulation of unlaid eggs also promotes the active state independent of the HSNs. The cholinergic VC motor neurons slow locomotion during egg-laying muscle contraction and egg release. The uv1 neuroendocrine cells mechanically sense passage of eggs through the vulva and release tyramine to inhibit egg laying, in part via the LGC-55 tyramine-gated Cl- channel on the HSNs. Our results identify discrete signals that entrain or detach the circuit from the locomotion central pattern generator to produce active and inactive states.https://elifesciences.org/articles/21126circuitneuromodulatorbehaviorserotonincalciumtyramine |
spellingShingle | Kevin M Collins Addys Bode Robert W Fernandez Jessica E Tanis Jacob C Brewer Matthew S Creamer Michael R Koelle Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition eLife circuit neuromodulator behavior serotonin calcium tyramine |
title | Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition |
title_full | Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition |
title_fullStr | Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition |
title_full_unstemmed | Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition |
title_short | Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition |
title_sort | activity of the c elegans egg laying behavior circuit is controlled by competing activation and feedback inhibition |
topic | circuit neuromodulator behavior serotonin calcium tyramine |
url | https://elifesciences.org/articles/21126 |
work_keys_str_mv | AT kevinmcollins activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT addysbode activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT robertwfernandez activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT jessicaetanis activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT jacobcbrewer activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT matthewscreamer activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition AT michaelrkoelle activityofthecelegansegglayingbehaviorcircuitiscontrolledbycompetingactivationandfeedbackinhibition |