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

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, V0 V ; inhibitory, V0 D ), 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.

Developmental switch in the function of inhibitory commissural V0d interneurons in zebrafish

“…V0d interneurons have been proposed to play a key role in controlling left-right alternation during locomotion in vertebrates, 22 particularly at slower speeds. 24,29 However, our results do not support such a role for these interneurons in larval zebrafish, given the negligible effect of their ablation on swimming behavior at these early stages, suggesting the involvement of other inhibitory commissural interneuron classes for slow swimming in zebrafish larvae (see discussion). To test whether V0d interneurons continue to play a role only in highspeed motor behavior in zebrafish throughout development, we carried out a similar behavioral analysis combined with two-photon ablation at juvenile/adult stages (4-7 wpf; Figure 3A).…”

“…22 However, the selective ablation of the V0 subclasses (V0d or V0v) has shown that they preferentially contribute to locomotor coordination in mice in a speed-dependent manner, with V0d interneurons controlling left-right limb alternation at slow walking speeds, whereas V0v interneurons perform this role at higher speeds during trotting. 24,29 In contrast to mice, V0d interneurons in larval zebrafish are active reliably only at the highest swimming speeds, 23 whereas MCoDs, a specific V0v interneuron type, are only active during slow swimming. 30,31 In adult zebrafish, V0v interneurons are largely recruited at higher speeds, as proposed in mice.…”

What Is the Brainstem Control of Locomotion?

“…They include various subtypes of glutamatergic, GABA/glycinergic, and local cholinergic interneurons that control the rhythmic activity of flexor and extensor motor neurons during the step and stance stages of locomotion. 32,[38][39][40][41] For example, commissural glutamatergic interneurons control right and left limb coordination during gait, 42,43 whereas a group of GABA/glycinergic neurons contribute to halting locomotion. 35 Spinal motor neurons contribute to control of the pattern of locomotion by providing real-time feedback from the motor unit.…”

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

“…Appropriate locomotor parameters are determined by the interplay of synaptic connections between excitatory and inhibitory interneurons in spinal CPG 1 , 2 , 7 , 8 . Recruitment of spinal glutamatergic interneurons, which project over many spinal segments, can generate locomotion 8 – 11 , set locomotor patterns 12 – 15 and coordinate the body’s rostral–caudal movement 5 , 16 . Spinal cord injury (SCI) causes locomotor dysfunction by severing the supraspinal connections as well as disrupting the neuronal network in spinal CPG 17 , 18 .…”