A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output
How neural circuits drive behavior is a central question in neuroscience. Proper execution of motor behavior requires precise coordination of many neurons. Within a motor circuit, individual neurons tend to play discrete roles by promoting or suppressing motor output. How exactly neurons function in...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-08-01
|
| Series: | Frontiers in Molecular Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnmol.2023.1228980/full |
| _version_ | 1827861568886407168 |
|---|---|
| author | Zhaoyu Li Zhaoyu Li Jiejun Zhou Jiejun Zhou Khursheed A. Wani Khursheed A. Wani Teng Yu Teng Yu Elizabeth A. Ronan Beverly J. Piggott Beverly J. Piggott Jianfeng Liu X.Z. Shawn Xu |
| author_facet | Zhaoyu Li Zhaoyu Li Jiejun Zhou Jiejun Zhou Khursheed A. Wani Khursheed A. Wani Teng Yu Teng Yu Elizabeth A. Ronan Beverly J. Piggott Beverly J. Piggott Jianfeng Liu X.Z. Shawn Xu |
| author_sort | Zhaoyu Li |
| collection | DOAJ |
| description | How neural circuits drive behavior is a central question in neuroscience. Proper execution of motor behavior requires precise coordination of many neurons. Within a motor circuit, individual neurons tend to play discrete roles by promoting or suppressing motor output. How exactly neurons function in specific roles to fine tune motor output is not well understood. In C. elegans, the interneuron RIM plays important yet complex roles in locomotion behavior. Here, we show that RIM both promotes and suppresses distinct features of locomotion behavior to fine tune motor output. This dual function is achieved via the excitation and inhibition of the same motor circuit by electrical and chemical neurotransmission, respectively. Additionally, this bi-directional regulation contributes to motor adaptation in animals placed in novel environments. Our findings reveal that individual neurons within a neural circuit may act in opposing ways to regulate circuit dynamics to fine tune behavioral output. |
| first_indexed | 2024-03-12T13:40:38Z |
| format | Article |
| id | doaj.art-d24e1fc9ce4344e3b7c19c0a85a6b7c6 |
| institution | Directory Open Access Journal |
| issn | 1662-5099 |
| language | English |
| last_indexed | 2024-03-12T13:40:38Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Molecular Neuroscience |
| spelling | doaj.art-d24e1fc9ce4344e3b7c19c0a85a6b7c62023-08-23T20:50:22ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992023-08-011610.3389/fnmol.2023.12289801228980A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor outputZhaoyu Li0Zhaoyu Li1Jiejun Zhou2Jiejun Zhou3Khursheed A. Wani4Khursheed A. Wani5Teng Yu6Teng Yu7Elizabeth A. Ronan8Beverly J. Piggott9Beverly J. Piggott10Jianfeng Liu11X.Z. Shawn Xu12Queensland Brain Institute, University of Queensland, St Lucia, QLD, AustraliaLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesCollege of Life Science and Technology, Key laboratory of Molecular Biophysics of MOE, International Research Center for Sensory Biology and Technology of MOST, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesDepartment of Microbiology and Physiological Systems, University of Massachusetts Medical School, Worcester, MA, United StatesLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesCollege of Life Science and Technology, Key laboratory of Molecular Biophysics of MOE, International Research Center for Sensory Biology and Technology of MOST, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesDivision of Biological Sciences, University of Montana, Missoula, MT, United StatesCollege of Life Science and Technology, Key laboratory of Molecular Biophysics of MOE, International Research Center for Sensory Biology and Technology of MOST, Huazhong University of Science and Technology, Wuhan, Hubei, ChinaLife Sciences Institute and Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, United StatesHow neural circuits drive behavior is a central question in neuroscience. Proper execution of motor behavior requires precise coordination of many neurons. Within a motor circuit, individual neurons tend to play discrete roles by promoting or suppressing motor output. How exactly neurons function in specific roles to fine tune motor output is not well understood. In C. elegans, the interneuron RIM plays important yet complex roles in locomotion behavior. Here, we show that RIM both promotes and suppresses distinct features of locomotion behavior to fine tune motor output. This dual function is achieved via the excitation and inhibition of the same motor circuit by electrical and chemical neurotransmission, respectively. Additionally, this bi-directional regulation contributes to motor adaptation in animals placed in novel environments. Our findings reveal that individual neurons within a neural circuit may act in opposing ways to regulate circuit dynamics to fine tune behavioral output.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1228980/fullmotor behaviormotor controlneural circuitC. elegansglutamate |
| spellingShingle | Zhaoyu Li Zhaoyu Li Jiejun Zhou Jiejun Zhou Khursheed A. Wani Khursheed A. Wani Teng Yu Teng Yu Elizabeth A. Ronan Beverly J. Piggott Beverly J. Piggott Jianfeng Liu X.Z. Shawn Xu A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output Frontiers in Molecular Neuroscience motor behavior motor control neural circuit C. elegans glutamate |
| title | A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| title_full | A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| title_fullStr | A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| title_full_unstemmed | A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| title_short | A C. elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| title_sort | c elegans neuron both promotes and suppresses motor behavior to fine tune motor output |
| topic | motor behavior motor control neural circuit C. elegans glutamate |
| url | https://www.frontiersin.org/articles/10.3389/fnmol.2023.1228980/full |
| work_keys_str_mv | AT zhaoyuli acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT zhaoyuli acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jiejunzhou acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jiejunzhou acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT khursheedawani acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT khursheedawani acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT tengyu acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT tengyu acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT elizabetharonan acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT beverlyjpiggott acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT beverlyjpiggott acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jianfengliu acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT xzshawnxu acelegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT zhaoyuli celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT zhaoyuli celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jiejunzhou celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jiejunzhou celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT khursheedawani celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT khursheedawani celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT tengyu celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT tengyu celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT elizabetharonan celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT beverlyjpiggott celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT beverlyjpiggott celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT jianfengliu celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput AT xzshawnxu celegansneuronbothpromotesandsuppressesmotorbehaviortofinetunemotoroutput |