Neuroethology of Melibe leonina swimming behavior

American Zoologist, Sep 2001 by Watson, Winsor H III, Lawrence, Kaddee A, Newcomb, James M

Neuroethology of Melibe leonina Swimming Behavior1

SYNOPSIS. The nudibranch Melibe leonina swims by rhythmically flexing its body from side to side at a frequency of I cycle every 2-5 sec. Melibe swim spontaneously, when they are dislodged from the substrate, or when they come in contact with predatory seastars, such as Pycnopodia helianthoides. Intracellular recordings obtained from semi-intact swimming Melibe reveal a population of ~15 swim motoneurons (SMNs) in each pedal ganglion. In general, SMNs in one pedal ganglion fire out-of-phase with SMNs in the opposite pedal ganglion, resulting in rhythmic side-to-side bending movements. In isolated brains, recordings from SMNs yield similar results, indicating the existence of a swim central pattern generator (CPG). There is no evidence for synaptic interactions between SMNs and either inhibiting or exciting SMNs has no impact on the swim pattern. The SMNs are driven by a CPG consisting of 4 interneurons; 2 in the cerebropleural ganglia and 1 in each pedal ganglion. Appropriate bursting activity in the swim interneurons is necessary for swimming to occur. Either hyperpolarization or depolarization of any of the 4 CPG interneurons disrupts the normal swim pattern. Swimming behavior, and the fictive swim motor program expressed by the isolated brain, are inhibited by light and nitric oxide donors. NADPH-diaphorase staining and nitric oxide synthase (NOS) immunocytochemistry of Melibe brains suggests the source of nitric oxide might be a pair of bilaterally symmetrical cells located in the cerebropleural ganglia.

INTRODUCTION

Crawling is the most common form of locomotion in opisthobranch molluscs, but at least 47 different species also swim, using five general kinds of swimming movements (Farmer, 1970). Of these five types of swimming, three are by far the most common: parapodial flapping, dorsal-ventral undulation, and lateral-bending.

The neural basis of opisthobranch swimming behavior has been investigated in several different opisthobranchs for decades because they have very large, identifiable, neurons that can be studied in both semiintact, moving preparations and inisolated brains. Of the four main species that have been examined, two swim by flapping their "wings" or parapodia (Clione limacina and Aplysia brasiliana) and two use dorsal-ventral flexions (Tritonia diomedea and Pleurobranchaea californica). Recently, we have been investigating the neuroethology of swimming in Melibe leonina, which swims using rhythmic lateral-bending movements. This manuscript is meant to provide a short review of previous studies concerning this subject and a summary of the results of ongoing investigations in our laboratory.

Although the neural basis of swimming in Melibe has received little attention until recently, a number of short descriptions of the behavior have appeared in the literature, going back to 1919 (Agersborg, 1919, 1921). These early papers provided descriptions of Melibe swimming, crawling, and feeding, as well as discussions of the adaptive significance of different forms of Melibe locomotion. In 1968 Ann Hurst published an excellent paper about various Melibe behaviors and she provided a good map of the brain along with accounts of some recordings obtained from a variety of neurons in the CNS. Recently, members of our laboratory have been carrying out further investigations of Melibe neuroethology, beginning with feeding behavior (Trimarchi and Watson, 1992; Watson and Trimarchi, 1992; Watson and Chester, 1993) and, more recently, extending to swimming behavior (Lawrence, 1997; Watson, 1997; Newcomb and Watson, 2001). This new information makes it possible to compare and contrast the neural basis of swimming in a lateralbending species with opisthobranchs that swim using parapodial flapping and dorsalventral flexions.

One of the major motivations for investigating the swimming behavior of opisthobranchs is that once we understand the neural circuits responsible for producing the behavior, we can then investigate how these circuits are modified by various stimuli or past experiences. We can also attempt to determine how these swim circuits overlap or interact with circuits for other behaviors, such as feeding and mating. In this Symposium there are a number of good examples of this type of analysis, ranging from the influence of serotonin on swimming in Tritonia and Clione, to the overlap between feeding and swimming circuits in Pleurobranchaea. Currently, we are studying how light and nitric oxide influence Melibe swimming and the underlying neural networks. In this short review we will provide some of this new evidence and discuss how the two processes might be related.

MATERIALS AND METHODS

Animals

Melibe were collected in the Puget Sound, WA, near the University of Washington's Friday Harbor Laboratories (FHL), on San Juan Island. Some experiments were carried out at FHL, while others were performed in the Zoology Department facilities at the University of New Hampshire.