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

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.

Kinematics of forward and backward locomotion performed in different environmental conditions.

Mice are frequently used in analyses of the locomotor system. Although forward locomotion (FWL) in intact mice has been studied previously, backward locomotion (BWL) in mice has never been analyzed. The aim of the present study was to compare kinematics of FWL and BWL performed in different environmental conditions (i.e., in a tunnel, on a treadmill, and on an air-ball). In all setups, the average speed and step amplitude during BWL were significantly reduced compared with FWL. The cycle duration varied greatly during both FWL and BWL. The average swing duration during BWL was twice shorter than during FWL on each setup. Mice exhibited different interlimb coordinations (trot and walk with lateral or diagonal sequence) during BWL but only one gait (walk with lateral sequence) during FWL. Location of the rostro-caudal paw trajectory in relation to the hip projection to the surface (HP) depended on hip height. With low hip height, the trajectory was displaced either rostrally (anterior steps) or caudally (posterior steps) to HP. With high hip height, HP was near the middle of the trajectory (middle steps). During FWL, all three forms of steps were observed in the tunnel and predominantly anterior and posterior steps on the treadmill and air-ball, respectively. During BWL, only anterior steps were observed. Intralimb coordination depended on the form of stepping. Limb joints were coordinated to keep the hip at approximately constant height during stance and to have the smallest functional limb length during swing when the limb passed under the hip.NEW & NOTEWORTHY Mice are extensively used for the analysis of the locomotor system. This study is the first examination of the kinematics of forward and backward locomotor movements in different environmental conditions in mice. Obtained results represent a benchmark for studies based on manipulations of activity of specific populations of neurons to reveal their roles in control of specific aspects of locomotion.