A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia
Locomotion in mollusc Aplysia is implemented by a pedal rolling wave, a type of axial locomotion. Well-studied examples of axial locomotion (pedal waves in Drosophila larvae and body waves in leech, lamprey, and fish) are generated in a segmented nervous system via activation of multiple coupled cen...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Association for the Advancement of Science (AAAS)
2023-01-01
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| Series: | Research |
| Online Access: | https://spj.science.org/doi/10.34133/research.0060 |
| _version_ | 1797227479170023424 |
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| author | Hui-Ying Wang Ke Yu Zhe Yang Guo Zhang Shi-Qi Guo Tao Wang Dan-Dan Liu Ruo-Nan Jia Yu-Tong Zheng Yan-Nan Su Yi Lou Klaudiusz R. Weiss Hai-Bo Zhou Feng Liu Elizabeth C. Cropper Quan Yu Jian Jing |
| author_facet | Hui-Ying Wang Ke Yu Zhe Yang Guo Zhang Shi-Qi Guo Tao Wang Dan-Dan Liu Ruo-Nan Jia Yu-Tong Zheng Yan-Nan Su Yi Lou Klaudiusz R. Weiss Hai-Bo Zhou Feng Liu Elizabeth C. Cropper Quan Yu Jian Jing |
| author_sort | Hui-Ying Wang |
| collection | DOAJ |
| description | Locomotion in mollusc Aplysia is implemented by a pedal rolling wave, a type of axial locomotion. Well-studied examples of axial locomotion (pedal waves in Drosophila larvae and body waves in leech, lamprey, and fish) are generated in a segmented nervous system via activation of multiple coupled central pattern generators (CPGs). Pedal waves in molluscs, however, are generated by a single pedal ganglion, and it is unknown whether there are single or multiple CPGs that generate rhythmic activity and phase shifts between different body parts. During locomotion in intact Aplysia, bursting activity in the parapedal commissural nerve (PPCN) was found to occur during tail contraction. A cluster of 20 to 30 P1 root neurons (P1Ns) on the ventral surface of the pedal ganglion, active during the pedal wave, were identified. Computational cluster analysis revealed that there are 2 phases to the motor program: phase I (centered around 168°) and phase II (centered around 357°). PPCN activity occurs during phase II. The majority of P1Ns are motoneurons. Coactive P1Ns tend to be electrically coupled. Two classes of pedal interneurons (PIs) were characterized. Class 1 (PI1 and PI2) is active during phase I. Their axons make a loop within the pedal ganglion and contribute to locomotor pattern generation. They are electrically coupled to P1Ns that fire during phase I. Class 2 (PI3) is active during phase II and innervates the contralateral pedal ganglion. PI3 may contribute to bilateral coordination. Overall, our findings support the idea that Aplysia pedal waves are generated by a single CPG. |
| first_indexed | 2024-03-13T07:12:43Z |
| format | Article |
| id | doaj.art-32acec8271c241319589ec38a975e9e9 |
| institution | Directory Open Access Journal |
| issn | 2639-5274 |
| language | English |
| last_indexed | 2024-04-24T14:41:27Z |
| publishDate | 2023-01-01 |
| publisher | American Association for the Advancement of Science (AAAS) |
| record_format | Article |
| series | Research |
| spelling | doaj.art-32acec8271c241319589ec38a975e9e92024-04-02T21:01:31ZengAmerican Association for the Advancement of Science (AAAS)Research2639-52742023-01-01610.34133/research.0060A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc AplysiaHui-Ying Wang0Ke Yu1Zhe Yang2Guo Zhang3Shi-Qi Guo4Tao Wang5Dan-Dan Liu6Ruo-Nan Jia7Yu-Tong Zheng8Yan-Nan Su9Yi Lou10Klaudiusz R. Weiss11Hai-Bo Zhou12Feng Liu13Elizabeth C. Cropper14Quan Yu15Jian Jing16State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.National Laboratory of Solid State Microstructures, Department of Physics, Institute for Brain Sciences, and Collaborative Innovation Center of Advanced Microstructures, Nanjing University, Nanjing, Jiangsu 210093, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.School of Electronic Science and Engineering, Nanjing University, Nanjing, Jiangsu 210023, China.National Laboratory of Solid State Microstructures, Department of Physics, Institute for Brain Sciences, and Collaborative Innovation Center of Advanced Microstructures, Nanjing University, Nanjing, Jiangsu 210093, China.Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.Peng Cheng Laboratory, Shenzhen 518000, China.State Key Laboratory of Pharmaceutical Biotechnology, Institute for Brain Sciences, Chinese Academy of Medical Sciences Research Unit of Extracellular RNA, Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, Advanced Institute for Life Sciences, Chemistry and Biomedicine Innovation Center, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China.Locomotion in mollusc Aplysia is implemented by a pedal rolling wave, a type of axial locomotion. Well-studied examples of axial locomotion (pedal waves in Drosophila larvae and body waves in leech, lamprey, and fish) are generated in a segmented nervous system via activation of multiple coupled central pattern generators (CPGs). Pedal waves in molluscs, however, are generated by a single pedal ganglion, and it is unknown whether there are single or multiple CPGs that generate rhythmic activity and phase shifts between different body parts. During locomotion in intact Aplysia, bursting activity in the parapedal commissural nerve (PPCN) was found to occur during tail contraction. A cluster of 20 to 30 P1 root neurons (P1Ns) on the ventral surface of the pedal ganglion, active during the pedal wave, were identified. Computational cluster analysis revealed that there are 2 phases to the motor program: phase I (centered around 168°) and phase II (centered around 357°). PPCN activity occurs during phase II. The majority of P1Ns are motoneurons. Coactive P1Ns tend to be electrically coupled. Two classes of pedal interneurons (PIs) were characterized. Class 1 (PI1 and PI2) is active during phase I. Their axons make a loop within the pedal ganglion and contribute to locomotor pattern generation. They are electrically coupled to P1Ns that fire during phase I. Class 2 (PI3) is active during phase II and innervates the contralateral pedal ganglion. PI3 may contribute to bilateral coordination. Overall, our findings support the idea that Aplysia pedal waves are generated by a single CPG.https://spj.science.org/doi/10.34133/research.0060 |
| spellingShingle | Hui-Ying Wang Ke Yu Zhe Yang Guo Zhang Shi-Qi Guo Tao Wang Dan-Dan Liu Ruo-Nan Jia Yu-Tong Zheng Yan-Nan Su Yi Lou Klaudiusz R. Weiss Hai-Bo Zhou Feng Liu Elizabeth C. Cropper Quan Yu Jian Jing A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia Research |
| title | A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia |
| title_full | A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia |
| title_fullStr | A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia |
| title_full_unstemmed | A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia |
| title_short | A Single Central Pattern Generator for the Control of a Locomotor Rolling Wave in Mollusc Aplysia |
| title_sort | single central pattern generator for the control of a locomotor rolling wave in mollusc aplysia |
| url | https://spj.science.org/doi/10.34133/research.0060 |
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