Figure 3.

A biophysical model for forward locomotion that integrates local oscillators, proprioceptive couplings and descending inputs from premotor interneurons. (a) The B-class motor neurons in the mid-body exhibited rhythmic calcium activities upon optogenetic activation of premotor interneuron AVBs. Note that imaging experiments were carried out in mutants unc-13 (e51) where chemical synaptic transmission in the whole nervous system was largely abolished. (b) Local and directional (anterior to posterior) proprioceptive couplings propagate body undulations. When a mid-body region of a worm was constrained in a straight microfluidic channel, the posterior body region emerged from the channel would remain still and straight. Curvature kymograph showed that the bending waves could only propagate to the anterior limit of the channel. When dynamic curvature change in the worm mid-body was imposed by a pneumatic microfluidic device, rapid curvature changes and bending waves followed in the posterior body. (c) Descending inputs from AVB interneurons are required for mid-body oscillations. Curvature kymographs show that, in an AVB-ablated worm, the bending amplitude decayed monotonically towards the tail during forward locomotion. When an anterior body region of a wild-type worm was immobilized via optogenetic inhibition of B-class motor neurons or muscle cells, higher frequency and low-amplitude bending waves emerged from the mid-body. Ablating AVB premotor interneurons would abolish the mid-body bending waves. (d) Local body oscillators, proprioceptive coupling between B-class motor neurons and AVB-B gap junction coupling work synergistically to drive and propagate a coordinated undulatory wave from the head to the tail. When a strong and time-varying proprioceptive signal from an anterior body region is absent, AVB-B gap junction coupling induces mid-body high-frequency undulation. In the absence of AVB-B gap junction inputs, proprioceptive couplings are less effective in propagating bending waves, leading to rapidly decaying bending amplitude towards the tail. Figure panels adapted from [40,41].