Neuroethology of Melibe leonina Swimming Behavior1

Abstract

SYNOPSIS. The nudibranch Melibe leonina swims by rhythmically flexing its body from side to side at a frequency of 1 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 ϳ15 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.

Central pattern generator for swimming in Melibe

“…These two cells have been named the right and left 'swim interneuron 1' (Rsint1 and Lsint1; referred to as SiI by Watson et al, 2001). Their cell bodies are located on the medial dorsal surface just caudal to the prominent tentacular lobe that rises from the center of the pleural ganglion (Fig.·1).…”

“…These two cells are termed the right and left 'swim interneuron 2' (Rsint2 and Lsint2; referred to as SiII by Watson et al, 2001). A single sint2 is found near the dorsal midline of each pedal ganglion (Fig.·1).…”

“…While this concept is widely accepted (Friesen, 1994), few examples of locomotor CPG networks are known in detail. The nudibranch mollusc Melibe leonina swims by bending from side to side in a behavior that can continue for hours in freely swimming animals (Hurst, 1968;Watson et al, 2001Watson et al, , 2002Lawrence and Watson, 2002). We studied the neural network responsible for generating the swimming rhythm in Melibe using microelectrode techniques applied to whole animal preparations, in which cellular activity and behavior could be recorded simultaneously.…”

Neural mechanisms underlying the evolvability of behaviour

“…Nudibranchs that do not swim like Tritonia or Pleurobranchaea also have homologues of the swim CPG neurons [119]. For example, Melibe leonina is more closely related to Tritonia than Pleurobranchaea, but swims by flexing its body from side to side instead of dorsally and ventrally [120,121] ( figure 3). This behaviour differs in several other fundamental ways from the Tritonia swim, including the duration of the episodes and the stimuli that will elicit the response.…”

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

“…The Tritonia swim is a high-threshold escape behaviour that is produced in response to only a few types of stimuli ( Willows 1967). Although the Melibe swim also functions as an escape response, it can occur spontaneously with no obvious stimulus, as a result of the animal simply being dislodged from the substrate, or in response to a decrease in ambient illumination ( Watson et al 2001;Lawrence & Watson 2002;Newcomb et al 2004). Furthermore, whereas a Tritonia swim episode lasts for less than a minute (Hume et al 1982), an episode of Melibe swimming can last for up to an hour (Mills 1994;Lawrence & Watson 2002;Caldwell & Donovan 2003).…”