Journal of Neuroscience, Vol 16, 2839-2859, Copyright © 1996 by Society for Neuroscience
Tests of the motor neuron model of the local pattern-generating circuits in the swimmeret system
CM Sherff and B Mulloney
Division of Biological Sciences, University of California, Davis, 95616- 8755, USA.
The motor pattern that drives each crayfish swimmeret consists of
alternating bursts of impulses in power-stroke (PS) and return-stroke (RS)
motor neurons. A model of the neural circuit that generates this pattern
focused on connections between motor neurons themselves (Heitler, 1978,
1981). The model predicts that synergist motor neurons are electrically
coupled, whereas antagonists make mostly inhibitory synapses. We tested
this model by observing the responses of motor neurons to pressure ejection
of GABA and glutamate, transmitters that crayfish motor neurons release at
neuromuscular junctions, and by measuring the strengths and delays of
synapses between pairs of motor neurons. Both GABA and glutamate inhibited
motor neurons. This inhibition persisted when synaptic transmitter release
was blocked by high Mg2+. The effects of GABA were mimicked by muscimol,
but not by baclofen or the GABAc receptor agonist cis-4-aminocrotonic acid,
and they were not blocked by bicuculline. The effects of glutamate were
mimicked by ibotenic acid. Picrotoxin partially blocked glutamate's
inhibition of the motor pattern, but did not affect GABA responses. Most
(87%) pairs of synergist motor neurons tested made weak, noninverting
connections. Approximately half of these had synaptic delays of <2 msec,
consistent with direct electrical or chemical synapses. Individual motor
neurons were dye-coupled to between one and three other motor neurons, and
to interneurons. Less than half (44%) of the pairs of antagonist motor
neurons tested made synaptic connections. These connections were weak, had
long latencies (>4 msec), and therefore were probably polysynaptic. We
conclude that direct synapses between swimmeret motor neurons cannot
account for alternation of PS and RS bursts.