Interneuronal Projections to Identified Cilia-Activating Pedal Neurons inHermissenda

Abstract

Neural networks have been shown to support the generation of more than one behavioral motor act. In the nudibranch mollusk Hermissenda, Pavlovian conditioning results in light, the conditioned stimulus (CS), evoking both inhibition of locomotion and foot contraction. The synaptic organization of the eyes and optic ganglion is well documented; however, the characterization of the neural network mediating visually modulated behaviors is incomplete. We have now characterized synaptic connections between identified photoreceptors and a newly identified interneuron (II(b)), identified synaptic projections from type I and type II interneurons to an inhibitory interneuron (III(i)) and to two newly identified pedal neurons, VP1 and VP2. Here we show that VP1 activates ciliary movement on the anterior foot and VP2 innervates the anterior foot and ventral tentacle. Stimulation of the photoreceptors with light produced two effects on the activity of VP1 and VP2. First, light inhibits type I(i) and II(i) interneurons and disinhibits VP1 and VP2. Depolarization of type II(e) interneurons also disinhibits VP1 and VP2. Second, the light-elicited depolarization and increased tonic activity of VP1 and VP2 is produced by excitatory synaptic input from ipsilateral and contralateral type II(b) interneurons. Pedal neurons VP1 and VP2 receive similar synaptic input from type I, II, and III(i) interneurons; this is in agreement with previous research showing that the visual pathway influences both ciliary locomotion and foot movement. The organization of the visual system in Hermissenda provides for the expression of cellular and synaptic plasticity supporting learning without altering the networks ability to carry out the requirements for normal visual processing.

Sensory Regulation of Network Components Underlying Ciliary Locomotion inHermissenda

“…Anatomical and electrophysiological criteria were used to identify type B photoreceptors, as described previously (Alkon 1973b;Alkon and Fuortes 1972;Crow and Tian 2000;Frysztak and Crow 1993). In isolated circumesophageal nervous systems, ciliary efferent neurons were identified based on soma size, position along the anterior-ventral edge of the pedal ganglion, electrophysiological responses to light stimulation of the photoreceptors, and extrinsic current stimulation of interneurons (Crow and Tian 2003a). In semi-intact preparations, ciliary efferent neurons were identified by recording ciliary movement evoked by depolarization of the neurons with extrinsic current (Crow and Tian 2003a).…”

“…Semi-intact preparations were prepared as described previously (Crow and Tian 2003a) by cooling the animals to between 0 and 1°C followed by isolation of the circumesophageal nervous system from the buccal crest and body leaving intact pedal nerves P1 and P2. The foot was positioned ventral side up adjacent to the isolated circumesophageal nervous system.…”

“…In contrast, the CPGs in the marine mollusks Pleurobranchaea and Tritonia support the generation of dissimilar behaviors; rhythmic escape swimming and nonrhythmic ciliary locomotion Gillette 1999, 2000;Popescu and Frost 2002). Ciliary locomotion or crawling is a nonmuscular, nonrhythmic gliding form of movement expressed in a number of mollusks (Audesirk 1978a,b;Copeland 1919Copeland , 1922Crow and Tian 2003a;Gainey 1976;Syed and Winlow 1989;Willows et al 1997). Identified components of the CPGs in Pleurobranchaea and Tritonia express rhythmic neural activity during escape swimming and tonic firing during ciliary locomotion (Jing and Gillette 2000;Popescu and Frost 2002).…”

“…Each identified A and B photoreceptor in the eye forms a monosynaptic connection with an aggregate of two distinct type I i interneurons (OFF-cells) and two type I e interneurons (ON-cells) (Crow andTian 2000, 2002b). The visual system modulates ciliary locomotion by the effect of illumination on the activity of type I e and I i interneurons projecting through polysynaptic pathways to type III i inhibitory interneurons that, in turn, regulate the firing of ciliary efferent neurons (Crow and Tian 2003a). Excitation of ciliary efferent neurons is also provided by synaptic input from type I b interneurons (Crow andTian 2003a, 2004).…”

Buccal neurons activate ciliary beating in the foregut of the pteropod molluskClione limacina

“…Neural control of cilia beating was described in the nudibranch mollusk Hermissenda (Crow and Tian, 2003) and the freshwater snail Planorbis corneus (Deliagina and Orlovsky, 1990) as well as in gastropod veliger larvae (Mackie et al, 1976) and the embryo of Helisoma trivolvis (Goldberg et al, 2008). Neural control of cilia was intensively studied in the nudibranch mollusk Tritonia diomedea.…”