TY - JOUR

T1 - Differential contribution of V0 interneurons to execution of rhythmic and non-rhythmic motor behaviors

AU - Zelenin, Pavel V

AU - Vemula, Manideep G

AU - Lyalka, Vladimir F

AU - Kiehn, Ole

AU - Talpalar, Adolfo E

AU - Deliagina, Tatiana G

N1 - Copyright © 2021 the authors.

PY - 2021

Y1 - 2021

N2 - 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, and 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 knockout 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 execution of scratching involves active inhibition of the contralateral scratching CPG mediated by excitatory V0 neurons. By contrast, other V0 subpopulations are elements of spinal networks generating postural corrections. Finally, all V0 subpopulations contribute to 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 the differential contribution of V0 subpopulations to diverse motor acts that provides new insight to organization of motor circuits.SIGNIFICANCE STATEMENTCommissural interneurons (CINs) 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, neuronal mechanisms underlying left-right coordination is unknown. Here, we demonstrate the functional role of excitatory V0 neurons and other sub-populations 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 context of different behaviors as well as in the anterior and posterior part of the body during a particular behavior.

AB - 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, and 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 knockout 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 execution of scratching involves active inhibition of the contralateral scratching CPG mediated by excitatory V0 neurons. By contrast, other V0 subpopulations are elements of spinal networks generating postural corrections. Finally, all V0 subpopulations contribute to 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 the differential contribution of V0 subpopulations to diverse motor acts that provides new insight to organization of motor circuits.SIGNIFICANCE STATEMENTCommissural interneurons (CINs) 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, neuronal mechanisms underlying left-right coordination is unknown. Here, we demonstrate the functional role of excitatory V0 neurons and other sub-populations 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 context of different behaviors as well as in the anterior and posterior part of the body during a particular behavior.

U2 - 10.1523/JNEUROSCI.1979-20.2021

DO - 10.1523/JNEUROSCI.1979-20.2021

M3 - Journal article

C2 - 33637562

VL - 41

SP - 3432

EP - 3445

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

SN - 0270-6474

IS - 15

ER -