Intersegmental coordination of the central pattern generator via interleaved electrical and chemical synapses in zebrafish spinal cord

A significant component of the repetitive dynamics during locomotion in vertebrates is generated within the spinal cord. The legged locomotion of mammals is most likely controled by a hierarchical, multi-layer spinal network structure, while the axial circuitry generating the undulatory swimming motion of animals like lamprey is thought to have only a single layer in each segment. Recent experiments have suggested a hybrid network structure in zebrafish larvae in which two types of excitatory interneurons (V2a-I and V2a-II) both make first-order connections to the brain and last-order connections to the motor pool. These neurons are connected by electrical and chemical synapses across segments. Through computational modeling and an asymptotic perturbation approach we show that this interleaved interaction between the two neuron populations allows the spinal network to quickly establish the correct activation sequence of the segments when starting from random initial conditions, as needed for a swimming spurt, and to reduce the dependence of the intersegmental phase difference (ISPD) of the oscillations on the swimming frequency. The latter reduces the frequency dependence of the waveform of the swimming motion. In the model the reduced frequency dependence is largely due to the different impact of chemical and electrical synapses on the ISPD and to the significant spike-frequency adaptation that has been observed experimentally in V2a-II neurons, but not in V2a-I neurons. Our model makes experimentally testable predictions and points to a benefit of the hybrid structure for undulatory locomotion that may not be relevant for legged locomotion.