During Fictive Locomotion, Graded Synaptic Currents Drive Bursts of Impulses in Swimmeret Motor Neurons

Abstract

During forward swimming, motor neurons that innervate each crayfish swimmeret fire periodic coordinated bursts of impulses. These bursts occur simultaneously in neurons that are functional synergists but alternate with bursts in their antagonists. These impulses ride on periodic oscillations of membrane potential that occur simultaneously in neurons of each type. A model of the local circuit that generates this motor pattern has been proposed. In this model, each motor neuron is driven alternately by excitatory and inhibitory synaptic currents from nonspiking local interneurons. I tested this model by perturbing individual interneurons and recording synaptic currents and changes in input resistance from each class of motor neuron. I also simulated the synaptic currents that would be observed in a cell subject to different patterns of presynaptic input. When the CNS was actively expressing the swimming motor pattern, changes in the membrane potential of individual local interneurons controlled firing of whole sets of motor neurons. Membrane currents in these motor neurons oscillated in phase with the motor output from their own local circuit. The phases of these oscillations differed in different functional classes of motor neurons. In neurons that could be clamped at the reversal potential of their outward currents, the model predicted that large periodic inward currents would be recorded. I observed no signs of periodic inward currents, even when the outward currents clearly had reversed. These results permit a simplification of the cellular model. They are discussed in the context of neural control of locomotion in crustacea and insects.