Excitatory and inhibitory activity in the dorsal musculature of the nematode Ascaris evoked by single dorsal excitatory motoneurons

Abstract

A physiological preparation, in which identified motoneurons of the nematode Ascaris lumbricoides can be individually stimulated, was used to map the response evoked by single dorsal excitatory (DE) motoneurons in muscle cells innervated along the length of the dorsal nerve cord. As previously reported (Walrond, J.P., I.S. Kass, A.O.W. Stretton, and J.E. Donmoyer (1985) J. Neurosci. 5: 1-8), stimulation of a DE cell produces excitatory responses in muscle cells which it directly innervates. Excitatory activity propagates along the most strongly activated region of muscle at a velocity of ~ 28 cm/sec, then relaxes into a slower velocity of ~ 12 cm/sec. When either the DE1 or DE3 neurons were stimulated, excitatory responses were also observed in muscle cells not directly innervated by the neuron. These signals propagate in the opposite direction from the fast-propagating activity at a velocity of ~ 13 cm/sec. Injection of hyperpolarizing current into muscle cells blocks this slower propagation but fails to block the faster conduction. We conclude that the fast-conducting responses result from signals propagating in the motor axon, whereas the slow responses are conducted through gap junctions which connect Ascaris muscle cells. Stimulating a single DE motoneuron also evokes hyperpolarizing muscle responses in regions adjacent to the zones of fast and slow excitation. Anatomically defined synapses from the DE motoneurons onto the dorsal inhibitor (DI) can account for this inhibition. DE-DI synaptic interactions combined with the reciprocal inhibitory circuit discussed in the preceding paper (Walrond, J.P. and A.O.W. Stretton (1985) J. Neurosci. 5: 9-15) provide the basis for a model which describes how a propagating wave of muscle contraction could be produced during nematode locomotion.