The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice
Speed-dependent interlimb coordination allows animals to maintain stable locomotion under different circumstances. The V3 neurons are known to be involved in interlimb coordination. We previously modeled the locomotor spinal circuitry controlling interlimb coordination (Danner et al., 2017). This mo...
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eLife Sciences Publications Ltd
2022-04-01
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| Online Access: | https://elifesciences.org/articles/73424 |
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| author | Han Zhang Natalia A Shevtsova Dylan Deska-Gauthier Colin Mackay Kimberly J Dougherty Simon M Danner Ying Zhang Ilya A Rybak |
| author_facet | Han Zhang Natalia A Shevtsova Dylan Deska-Gauthier Colin Mackay Kimberly J Dougherty Simon M Danner Ying Zhang Ilya A Rybak |
| author_sort | Han Zhang |
| collection | DOAJ |
| description | Speed-dependent interlimb coordination allows animals to maintain stable locomotion under different circumstances. The V3 neurons are known to be involved in interlimb coordination. We previously modeled the locomotor spinal circuitry controlling interlimb coordination (Danner et al., 2017). This model included the local V3 neurons that mediate mutual excitation between left and right rhythm generators (RGs). Here, our focus was on V3 neurons involved in ascending long propriospinal interactions (aLPNs). Using retrograde tracing, we revealed a subpopulation of lumbar V3 aLPNs with contralateral cervical projections. V3OFF mice, in which all V3 neurons were silenced, had a significantly reduced maximal locomotor speed, were unable to move using stable trot, gallop, or bound, and predominantly used a lateral-sequence walk. To reproduce this data and understand the functional roles of V3 aLPNs, we extended our previous model by incorporating diagonal V3 aLPNs mediating inputs from each lumbar RG to the contralateral cervical RG. The extended model reproduces our experimental results and suggests that locally projecting V3 neurons, mediating left–right interactions within lumbar and cervical cords, promote left–right synchronization necessary for gallop and bound, whereas the V3 aLPNs promote synchronization between diagonal fore and hind RGs necessary for trot. The model proposes the organization of spinal circuits available for future experimental testing. |
| first_indexed | 2024-12-10T04:29:11Z |
| format | Article |
| id | doaj.art-42d61dd4982246aeafa0423e47279086 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:29:11Z |
| publishDate | 2022-04-01 |
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| spelling | doaj.art-42d61dd4982246aeafa0423e472790862022-12-22T02:02:12ZengeLife Sciences Publications LtdeLife2050-084X2022-04-011110.7554/eLife.73424The role of V3 neurons in speed-dependent interlimb coordination during locomotion in miceHan Zhang0https://orcid.org/0000-0001-5494-3504Natalia A Shevtsova1https://orcid.org/0000-0002-1971-9707Dylan Deska-Gauthier2Colin Mackay3Kimberly J Dougherty4https://orcid.org/0000-0002-0807-574XSimon M Danner5https://orcid.org/0000-0002-4642-7064Ying Zhang6https://orcid.org/0000-0003-4363-5666Ilya A Rybak7https://orcid.org/0000-0003-3461-349XDepartment of Medical Neuroscience, Brain Repair Centre, Faculty of Medicine, Dalhousie University, Halifax, CanadaDepartment of Neurobiology and Anatomy, College of Medicine, Drexel University, Philadelphia, United StatesDepartment of Medical Neuroscience, Brain Repair Centre, Faculty of Medicine, Dalhousie University, Halifax, CanadaDepartment of Medical Neuroscience, Brain Repair Centre, Faculty of Medicine, Dalhousie University, Halifax, CanadaDepartment of Neurobiology and Anatomy, College of Medicine, Drexel University, Philadelphia, United StatesDepartment of Neurobiology and Anatomy, College of Medicine, Drexel University, Philadelphia, United StatesDepartment of Medical Neuroscience, Brain Repair Centre, Faculty of Medicine, Dalhousie University, Halifax, CanadaDepartment of Neurobiology and Anatomy, College of Medicine, Drexel University, Philadelphia, United StatesSpeed-dependent interlimb coordination allows animals to maintain stable locomotion under different circumstances. The V3 neurons are known to be involved in interlimb coordination. We previously modeled the locomotor spinal circuitry controlling interlimb coordination (Danner et al., 2017). This model included the local V3 neurons that mediate mutual excitation between left and right rhythm generators (RGs). Here, our focus was on V3 neurons involved in ascending long propriospinal interactions (aLPNs). Using retrograde tracing, we revealed a subpopulation of lumbar V3 aLPNs with contralateral cervical projections. V3OFF mice, in which all V3 neurons were silenced, had a significantly reduced maximal locomotor speed, were unable to move using stable trot, gallop, or bound, and predominantly used a lateral-sequence walk. To reproduce this data and understand the functional roles of V3 aLPNs, we extended our previous model by incorporating diagonal V3 aLPNs mediating inputs from each lumbar RG to the contralateral cervical RG. The extended model reproduces our experimental results and suggests that locally projecting V3 neurons, mediating left–right interactions within lumbar and cervical cords, promote left–right synchronization necessary for gallop and bound, whereas the V3 aLPNs promote synchronization between diagonal fore and hind RGs necessary for trot. The model proposes the organization of spinal circuits available for future experimental testing.https://elifesciences.org/articles/73424locomotionspinal cordcetral pattern generatorcommissural interneuronslong propriospinal neuronscomputational modeling |
| spellingShingle | Han Zhang Natalia A Shevtsova Dylan Deska-Gauthier Colin Mackay Kimberly J Dougherty Simon M Danner Ying Zhang Ilya A Rybak The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice eLife locomotion spinal cord cetral pattern generator commissural interneurons long propriospinal neurons computational modeling |
| title | The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice |
| title_full | The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice |
| title_fullStr | The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice |
| title_full_unstemmed | The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice |
| title_short | The role of V3 neurons in speed-dependent interlimb coordination during locomotion in mice |
| title_sort | role of v3 neurons in speed dependent interlimb coordination during locomotion in mice |
| topic | locomotion spinal cord cetral pattern generator commissural interneurons long propriospinal neurons computational modeling |
| url | https://elifesciences.org/articles/73424 |
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