Command neurons for locomotion in Aplysia.

1. Command neurons for the pedal wave motor program (PWMP) that drives locomotion in Aplysia were examined electrophysiologically in the isolated nervous system. The cerebral ganglion contained a minimum of four command (type I) neurons that were excited by stimuli known to trigger locomotion in vivo and evoke its neural correlates in vitro. 2. Type I neurons fired during both spontaneous and sensory evoked pedal wave motor program bursting in pedal nerves and motor neurons. Intracellular stimulation of type I neurons at physiological frequencies (2-8 Hz) was sufficient to initiate the pedal wave motor program in quiescent preparations. 3. Increasing the type I neuron firing frequency decreased both the latency to the first pedal wave burst and the period of ongoing bursts. Driving type I neurons maintained the motor program as long as the stimulation continued. Repeated type I neuron stimulation caused decrement of the evoked motor program. 4. Hyperpolarizing type I neurons blocked both spontaneous and sensory evoked pedal wave motor program bursting. Type I neurons thus appeared to be true command neurons, being both sufficient and probably necessary for pedal wave motor program generation. 5. The command neurons exhibited similar firing patterns due to common synaptic input. They were not monosynaptically or electronically coupled and exhibited reciprocal recurrent inhibition among themselves. Driving one command neuron inhibited the others, indicating that they were individually sufficient and did not function as a mutually excited network. Thus they constitute a redundant command system. 6. There were no direct synaptic connections between the command neurons and pedal motor neurons. The command neurons did receive excitatory synaptic input during pedal wave bursts, indicating positive feedback from the oscillator. 7. In addition to the type I neurons, other neurons were found that appeared to have a modulatory function. Type II neurons could also initiate weak bursting but did not appear necessary for motor program generation. Types IIIA and IIIB neurons, respectively, monosynaptically excited and inhibited pedal motor neurons but could not initiate pedal wave bursting. Type IIIC neurons appeared to inhibit the pedal wave oscillator. The organization of the cerebral command and modulatory neurons in the control of locomotion was considered.