Sensory Regulation of Network Components Underlying Ciliary Locomotion inHermissenda

Abstract

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 Ii(off-cell) spike activity, excitation of type Ie(on-cell) spike activity, decreased spike activity in type IIIiinhibitory interneurons, and increased spike activity of ciliary efferent neurons. Here we show that pairs of type Iiinterneurons and pairs of type Ieinterneurons are electrically coupled. Neither electrical coupling or synaptic connections were observed between Ieand Iiinterneurons. Coupling is effective in synchronizing dark-adapted spontaneous firing between pairs of Ieand pairs of Iiinterneurons. Out-of-phase burst activity, occasionally observed in dark-adapted and light-adapted pairs of Ieand Iiinterneurons, 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 Ieand Iiinterneurons 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.