Literature DB >> 33637562

Differential Contribution of V0 Interneurons to Execution of Rhythmic and Nonrhythmic Motor Behaviors.

Pavel V Zelenin1, Manideep G Vemula1, Vladimir F Lyalka1, Ole Kiehn1,2, Adolfo E Talpalar3, Tatiana G Deliagina3.   

Abstract

Locomotion, scratching, and stabilization of the body orientation in space are basic motor functions which are critically important for animal survival. Their execution requires coordinated activity of muscles located in the left and right halves of the body. Commissural interneurons (CINs) are critical elements of the neuronal networks underlying the left-right motor coordination. V0 interneurons (characterized by the early expression of the transcription factor Dbx1) contain a major class of CINs in the spinal cord (excitatory, V0V; inhibitory, V0D), and a small subpopulation of excitatory ipsilaterally projecting interneurons. The role of V0 CINs in left-right coordination during forward locomotion was demonstrated earlier. Here, to reveal the role of glutamatergic V0 and other V0 subpopulations in control of backward locomotion, scratching, righting behavior, and postural corrections, kinematics of these movements performed by wild-type mice and knock-out mice with glutamatergic V0 or all V0 interneurons ablated were compared. Our results suggest that the functional effect of excitatory V0 neurons during backward locomotion and scratching is inhibitory, and that the execution of scratching involves active inhibition of the contralateral scratching central pattern generator mediated by excitatory V0 neurons. By contrast, other V0 subpopulations are elements of spinal networks generating postural corrections. Finally, all V0 subpopulations contribute to the generation of righting behavior. We found that different V0 subpopulations determine left-right coordination in the anterior and posterior parts of the body during a particular behavior. Our study shows a differential contribution of V0 subpopulations to diverse motor acts that provides new insight to organization of motor circuits.SIGNIFICANCE STATEMENT Commissural interneurons with their axons crossing the midline of the nervous system are critical elements of the neuronal networks underlying the left-right motor coordination. For the majority of motor behaviors, the neuronal mechanisms underlying left-right coordination are unknown. Here, we demonstrate the functional role of excitatory V0 neurons and other subpopulations of V0 interneurons in control of a number of basic motor behaviors-backward locomotion, scratching, righting behavior, and postural corrections-which are critically important for animal survival. We have shown that different subpopulations of V0 neurons determine left-right coordination in the context of different behaviors as well as in the anterior and posterior parts of the body during a particular behavior.
Copyright © 2021 the authors.

Entities:  

Keywords:  commissural interneurons; locomotion; mice; networks; posture; scratching

Year:  2021        PMID: 33637562      PMCID: PMC8051683          DOI: 10.1523/JNEUROSCI.1979-20.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  62 in total

1.  Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator.

Authors:  Simon J B Butt; Ronald M Harris-Warrick; Ole Kiehn
Journal:  J Neurosci       Date:  2002-11-15       Impact factor: 6.167

2.  Role of different sensory inputs for maintenance of body posture in sitting rat and rabbit.

Authors:  T Deliagina; I N Beloozerova; L B Popova; M G Sirota; H A Swadlow; G Grant; G N Orlovsky
Journal:  Motor Control       Date:  2000-10       Impact factor: 1.422

3.  V1 spinal neurons regulate the speed of vertebrate locomotor outputs.

Authors:  Simon Gosgnach; Guillermo M Lanuza; Simon J B Butt; Harald Saueressig; Ying Zhang; Tomoko Velasquez; Dieter Riethmacher; Edward M Callaway; Ole Kiehn; Martyn Goulding
Journal:  Nature       Date:  2006-03-09       Impact factor: 49.962

4.  Interlimb postural coordination in the standing cat.

Authors:  Tatiana G Deliagina; Mikhail G Sirota; Pavel V Zelenin; Grigori N Orlovsky; Irina N Beloozerova
Journal:  J Physiol       Date:  2006-03-09       Impact factor: 5.182

5.  [Central pathway of the scratch reflex in cats].

Authors:  T G Deliagina
Journal:  Neirofiziologiia       Date:  1977

6.  Projection patterns of lamina VIII commissural neurons in the lumbar spinal cord of the adult cat: an anterograde neural tracing study.

Authors:  K Matsuyama; S Kobayashi; M Aoki
Journal:  Neuroscience       Date:  2006-03-13       Impact factor: 3.590

Review 7.  Decoding the organization of spinal circuits that control locomotion.

Authors:  Ole Kiehn
Journal:  Nat Rev Neurosci       Date:  2016-03-03       Impact factor: 34.870

8.  In mice lacking V2a interneurons, gait depends on speed of locomotion.

Authors:  Steven A Crone; Guisheng Zhong; Ronald Harris-Warrick; Kamal Sharma
Journal:  J Neurosci       Date:  2009-05-27       Impact factor: 6.167

9.  V3 spinal neurons establish a robust and balanced locomotor rhythm during walking.

Authors:  Ying Zhang; Sujatha Narayan; Eric Geiman; Guillermo M Lanuza; Tomoko Velasquez; Bayle Shanks; Turgay Akay; Jason Dyck; Keir Pearson; Simon Gosgnach; Chen-Ming Fan; Martyn Goulding
Journal:  Neuron       Date:  2008-10-09       Impact factor: 17.173

10.  Spinal and supraspinal control of the direction of stepping during locomotion.

Authors:  Pavel E Musienko; Pavel V Zelenin; Vladimir F Lyalka; Yury P Gerasimenko; Grigory N Orlovsky; Tatiana G Deliagina
Journal:  J Neurosci       Date:  2012-11-28       Impact factor: 6.167

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  3 in total

1.  Activity of Spinal Interneurons during Forward and Backward Locomotion.

Authors:  Pavel E Musienko; Vladimir F Lyalka; Oleg V Gorskii; Pavel V Zelenin; Tatiana G Deliagina
Journal:  J Neurosci       Date:  2022-03-16       Impact factor: 6.709

2.  An injury-induced serotonergic neuron subpopulation contributes to axon regrowth and function restoration after spinal cord injury in zebrafish.

Authors:  Na N Guan; Jianren Song; Chun-Xiao Huang; Yacong Zhao; Jie Mao; Zhen Wang; Lulu Xu; Jianwei Cheng
Journal:  Nat Commun       Date:  2021-12-07       Impact factor: 14.919

3.  Induction of Ventral Spinal V0 Interneurons from Mouse Embryonic Stem Cells.

Authors:  Jennifer Pardieck; Manwal Harb; Shelly Sakiyama-Elbert
Journal:  Stem Cells Dev       Date:  2021-07-16       Impact factor: 4.390

  3 in total

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