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Sensory Regulation of Network Components Underlying Ciliary Locomotion in Hermissenda

Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas

Submitted 11 July 2008; accepted in final form 29 August 2008

Ciliary locomotion in the nudibranch mollusk Hermissenda is modulated by the visual and graviceptive systems. Components of the neural network mediating ciliary locomotion have been identified including aggregates of polysensory interneurons that receive monosynaptic input from identified photoreceptors and efferent neurons that activate cilia. Illumination produces an inhibition of type I_i (OFF-cell) spike activity, excitation of type I_e (ON-cell) spike activity, decreased spike activity in type III_i inhibitory interneurons, and increased spike activity of ciliary efferent neurons. Here we show that pairs of type I_i interneurons and pairs of type I_e interneurons are electrically coupled. Neither electrical coupling or synaptic connections were observed between I_e and I_i interneurons. Coupling is effective in synchronizing dark-adapted spontaneous firing between pairs of I_e and pairs of I_i interneurons. Out-of-phase burst activity, occasionally observed in dark-adapted and light-adapted pairs of I_e and I_i interneurons, suggests that they receive synaptic input from a common presynaptic source or sources. Rhythmic activity is typically not a characteristic of dark-adapted, light-adapted, or light-evoked firing of type I interneurons. However, burst activity in I_e and I_i interneurons may be elicited by electrical stimulation of pedal nerves or generated at the offset of light. Our results indicate that type I interneurons can support the generation of both rhythmic activity and changes in tonic firing depending on sensory input. This suggests that the neural network supporting ciliary locomotion may be multifunctional. However, consistent with the nonmuscular and nonrhythmic characteristics of visually modulated ciliary locomotion, type I interneurons exhibit changes in tonic activity evoked by illumination.