Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice
Summary: While considerable progress has been made in understanding the neuronal circuits that underlie the patterning of locomotor behaviors, less is known about the circuits that amplify motoneuron output to adjust muscle force. Here, we demonstrate that propriospinal V3 neurons (Sim1+) account fo...
Saved in:
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2025-01-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124724015638 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1841533363822788608 |
|---|---|
| author | Han Zhang Dylan Deska-Gauthier Colin S. MacKay Krishnapriya Hari Ana M. Lucas-Osma Joanna Borowska-Fielding Reese L. Letawsky Vladimir Rancic Turgay Akay Keith K. Fenrich David J. Bennett Ying Zhang |
| author_facet | Han Zhang Dylan Deska-Gauthier Colin S. MacKay Krishnapriya Hari Ana M. Lucas-Osma Joanna Borowska-Fielding Reese L. Letawsky Vladimir Rancic Turgay Akay Keith K. Fenrich David J. Bennett Ying Zhang |
| author_sort | Han Zhang |
| collection | DOAJ |
| description | Summary: While considerable progress has been made in understanding the neuronal circuits that underlie the patterning of locomotor behaviors, less is known about the circuits that amplify motoneuron output to adjust muscle force. Here, we demonstrate that propriospinal V3 neurons (Sim1+) account for ∼20% of excitatory input to motoneurons across hindlimb muscles. V3 neurons also form extensive connections among themselves and with other excitatory premotor neurons, such as V2a neurons. Optical activation of V3 neurons in a single segment rapidly amplifies locomotor-related motoneuron output at all lumbar segments in in vitro spinal cord and the awake adult mouse. Despite similar innervation from V3 neurons to flexor and extensor motoneuron pools, V3 neurons preferentially activate extensor muscles. Genetically or optogenetically silencing V3 neurons leads to slower and weaker mice with a reduced ability to adjust extensor muscle force. Thus, V3 neurons serve as global command neurons that amplify locomotion intensity. |
| format | Article |
| id | doaj-art-e6a44dcb38a74d1ab731ae5c8c5461ba |
| institution | Kabale University |
| issn | 2211-1247 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj-art-e6a44dcb38a74d1ab731ae5c8c5461ba2025-01-16T04:28:35ZengElsevierCell Reports2211-12472025-01-01441115212Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in miceHan Zhang0Dylan Deska-Gauthier1Colin S. MacKay2Krishnapriya Hari3Ana M. Lucas-Osma4Joanna Borowska-Fielding5Reese L. Letawsky6Vladimir Rancic7Turgay Akay8Keith K. Fenrich9David J. Bennett10Ying Zhang11Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, Canada; Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB T6G 2G4, Canada; Department of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, CanadaDepartment of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, CanadaDepartment of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, Canada; Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB T6G 2G4, CanadaDepartment of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, Canada; Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB T6G 2G4, Canada; Institute for Smart Augmentative and Restorative Technologies, University of Alberta, Edmonton, AB T6G 1G7, CanadaDepartment of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, Canada; Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB T6G 2G4, Canada; Institute for Smart Augmentative and Restorative Technologies, University of Alberta, Edmonton, AB T6G 1G7, CanadaNeuroscience and Mental Health Institute, University of Alberta, Edmonton, AB T6G 2S2, Canada; Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB T6G 2G4, CanadaDepartment of Medical Neuroscience, Dalhousie University, Halifax, NS B3H 4R2, Canada; Corresponding authorSummary: While considerable progress has been made in understanding the neuronal circuits that underlie the patterning of locomotor behaviors, less is known about the circuits that amplify motoneuron output to adjust muscle force. Here, we demonstrate that propriospinal V3 neurons (Sim1+) account for ∼20% of excitatory input to motoneurons across hindlimb muscles. V3 neurons also form extensive connections among themselves and with other excitatory premotor neurons, such as V2a neurons. Optical activation of V3 neurons in a single segment rapidly amplifies locomotor-related motoneuron output at all lumbar segments in in vitro spinal cord and the awake adult mouse. Despite similar innervation from V3 neurons to flexor and extensor motoneuron pools, V3 neurons preferentially activate extensor muscles. Genetically or optogenetically silencing V3 neurons leads to slower and weaker mice with a reduced ability to adjust extensor muscle force. Thus, V3 neurons serve as global command neurons that amplify locomotion intensity.http://www.sciencedirect.com/science/article/pii/S2211124724015638CP: Neuroscience |
| spellingShingle | Han Zhang Dylan Deska-Gauthier Colin S. MacKay Krishnapriya Hari Ana M. Lucas-Osma Joanna Borowska-Fielding Reese L. Letawsky Vladimir Rancic Turgay Akay Keith K. Fenrich David J. Bennett Ying Zhang Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice Cell Reports CP: Neuroscience |
| title | Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice |
| title_full | Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice |
| title_fullStr | Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice |
| title_full_unstemmed | Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice |
| title_short | Widespread innervation of motoneurons by spinal V3 neurons globally amplifies locomotor output in mice |
| title_sort | widespread innervation of motoneurons by spinal v3 neurons globally amplifies locomotor output in mice |
| topic | CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2211124724015638 |
| work_keys_str_mv | AT hanzhang widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT dylandeskagauthier widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT colinsmackay widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT krishnapriyahari widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT anamlucasosma widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT joannaborowskafielding widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT reeselletawsky widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT vladimirrancic widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT turgayakay widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT keithkfenrich widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT davidjbennett widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice AT yingzhang widespreadinnervationofmotoneuronsbyspinalv3neuronsgloballyamplifieslocomotoroutputinmice |