Coordination of startle and swimming neural systems in the pteropod mollusk Clione limacina: role of the cerebral cholinergic interneuron.

The holoplanktonic pteropod mollusk Clione limacina has a unique startle system that provides a very fast, ballistic movement of the animal during escape or prey capture behaviors. The startle system consists of two groups of large pedal motoneurons that control ventral or dorsal flexions of the wings. Although startle motoneurons innervate the same musculature used during normal swimming, they are independent of the swim central pattern generator and swim motoneurons. This study demonstrates that a cerebral startle (Cr-St) interneuron, which provides prominent excitatory inputs to startle motoneurons, plays a very important role in coordination of the startle and swimming neural systems. The Cr-St interneuron produces, simultaneously with monosynaptic excitatory inputs to dorsal startle motoneurons, monosynaptic inhibitory inputs to all types of swim neurons, including interneurons of the central pattern generator, general excitor motoneurons, small motoneurons, and modulatory pedal serotonergic wing neurons. The inhibitory synaptic transmission between the Cr-St interneuron and swim interneurons and motoneurons, as well as excitatory transmission between the Cr-St interneuron and startle motoneurons, appears to be cholinergic because it is blocked by the cholinergic antagonists atropine and d-tubocurarine, mimicked by exogenous acetylcholine in very low concentrations, and enhanced by the cholinesterase inhibitor eserine (physostigmine). The Cr-St-neuron-mediated inhibitory inputs to the swimming system are strong enough to completely terminate swimming activity while the Cr-St interneuron is active. Mechanosensory inputs are capable of triggering Cr-St neuron firing at rates sufficient to suppress fictive swimming in reduced preparations. Thus the Cr-St interneuron can temporally remove the swimming system from the control over the swim musculature while simultaneously activating the startle system to produce a powerful, short-latency response.