Network interneurons underlying ciliary locomotion inHermissenda

Abstract

In the nudibranch mollusk Hermissenda, ciliary locomotion contributes to the generation of two tactic behaviors. Light elicits a positive phototaxis, and graviceptive stimulation evokes a negative gravitaxis. Two classes of light-responsive premotor interneurons in the network contributing to ciliary locomotion have been recently identified in the cerebropleural ganglia. Aggregates of type I interneurons receive monosynaptic excitatory (Ie) or inhibitory (Ii) input from identified photoreceptors. Type II interneurons receive polysynaptic excitatory (IIe) or inhibitory (IIi) input from photoreceptors. The ciliary network also includes type III inhibitory (IIIi) interneurons, which form monosynaptic inhibitory connections with ciliary efferent neurons (CENs). Illumination of the eyes evokes a complex inhibitory postsynaptic potential, a decrease of Iispike activity, a complex excitatory postsynaptic potential, and an increase of Iespike activity. Here, we characterized the contribution of identified I, II, and IIIiinterneurons to the neural network supporting visually guided locomotion. In dark-adapted preparations, light elicited an increase in the tonic spike activity of IIeinterneurons and a decrease in the tonic spike activity of IIiinterneurons. Fluorescent dye-labeled type II interneurons exhibited diverse projections within the circumesophageal nervous system. However, a subclass of type II interneurons, IIe(cp)and IIi(cp)interneurons, were shown to terminate within the ipsilateral cerebropleural ganglia and indirectly modulate the activity of CENs. Type II interneurons form monosynaptic or polysynaptic connections with previously identified components of the ciliary network. The identification of a monosynaptic connection between Ieand IIIiinterneurons shown here suggest that they provide a major role in the light-dependent modulation of CEN spike activity underlying ciliary locomotion.