The Journal of Neuroscience, July 2, 2003, 23(13):5953-5962
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During Fictive Locomotion, Graded Synaptic Currents Drive Bursts of Impulses in Swimmeret Motor Neurons
Brian Mulloney
Section of Neurobiology, Physiology, and Behavior, University of
California, Davis, California 95616-8519
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.
Key words: graded transmission; synaptic inhibition; coordination; locomotion; nonspiking local interneuron; bursting
Received Feb. 19, 2003;
revised Apr. 15, 2003;
accepted May. 6, 2003.
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