Sensory Regulation of Network Components Underlying Ciliary Locomotion inHermissenda

Abstract

Crow T, Tian L-M. Sensory regulation of network components underlying ciliary locomotion in Hermissenda. J Neurophysiol 100: 2496 -2506, 2008. First published September 3, 2008 doi:10.1152/jn.90759.2008. 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.

Network interneurons underlying ciliary locomotion inHermissenda

“…This indicates that in addition to their contribution to the network supporting ciliary locomotion, type II interneurons are also involved in other light-dependent processes based on their anatomic projections and not differences in light responses. The spike activity of dark-adapted and light-adapted type II interneurons is tonic, which is consistent with the nonrhythmic spike activity of I e and I i interneurons recorded in the dark and during illumination (Crow and Tian 2008).…”

“…Spike activity was examined in II e (n ϭ 10) and II i (n ϭ 10) interneurons before (dark adapted) and during 5 min of illumination of the eyes (light adapted) to characterize light responses under conditions of illumination supporting phototactic behavior. Previous results have shown that the spike activity of dark-adapted type I e and I i interneurons is characterized by a change in tonic firing with the generation of occasional irregular burst activity that is not repetitive or rhythmic (Crow and Tian 2008). Group summary data showing the mean spike frequency measured at consecutive 1-min periods, 5 min before light onset, during 5 min of light, and 5 min after light offset are shown in Fig.…”

“…Polysensory type I b interneurons are excited by graviceptive input sufficient to generate foot contractions and ciliary activity, but are not typically activated by visual input Tian 2004, 2009). In contrast, the network supporting visually guided locomotion involves two classes of lightresponsive interneurons in the cerebropleural ganglia that are weakly excited by mechanical stimulation of the statocysts (Akaike and Alkon 1980;Goh and Alkon 1984;Crow and Tian 2000, 2008. The first class of light-responsive premotor interneurons, designated as type I, receive monosynaptic input from identified photoreceptors (Crow and Tian 2000, 2008.…”

“…In contrast, the network supporting visually guided locomotion involves two classes of lightresponsive interneurons in the cerebropleural ganglia that are weakly excited by mechanical stimulation of the statocysts (Akaike and Alkon 1980;Goh and Alkon 1984;Crow and Tian 2000, 2008. The first class of light-responsive premotor interneurons, designated as type I, receive monosynaptic input from identified photoreceptors (Crow and Tian 2000, 2008. Type II interneurons are a second group of light-responsive interneurons that receive polysynaptic input from photoreceptors (Crow and Tian 2002).…”

“…The visual system contributes to ciliary locomotion by light-dependent modulation of the spike activity of type I excitatory (I e ), type I inhibitory (I i ), type II excitatory (II e ), type II inhibitory (II i ), and type III inhibitory (III i ) interneurons that regulate the firing of CENs (Crow and Tian 2003). The light-adapted activity of I e and I i interneurons has been examined in detail, and the synaptic interactions between identified photoreceptors and I e -I i interneurons, III i interneurons, and CENs are well documented (Crow and Tian 2000, 2008. However, little is known about light-adapted activity of type II interneurons, their synaptic connections within the network supporting light-elicited ciliary activity, or potential direct excitatory/inhibitory connections with CENs.…”