Neuroethology of Melibe leonina swimming behavior

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

Comparisons between neural circuits underlying lateral-bending swimming vs. other types of opisthobranch swimming

It would appear, based on our current knowledge of the Melibe swim circuit, that it is relatively simple in comparison with the other known opisthobranch swim circuits. The CPG consists of only 4 interneurons, which, due to electrical coupling, function as a pair that reciprocally inhibit each other. In this respect, the Melibe circuit is somewhat similar to the Clione circuit. Both Tritona and Pleurobranchaea, which swim with dorsal-ventral flexions, have a much more intricate CPG, involving more neurons and more complex synaptic interactions (Getting, 1980; Getting et al., 1980; Lennard et al., 1980; Jing and Gillette, 1995, 1999; Katz, et al., 2001; Frost et al., 2001, Gillette and Jing, 2001). In Clione, an almost continuous parapodial swimmer, the basic CPG is fairly simple (Satterlie, 1985; Arshavsky et al., 1985). But because the circuit is also involved in other types of behaviors, and can change speeds, the overall swim circuit is more complex (Satterlie, 1991; Norekian, 1995; Satterlie and Norekian, 2001; Norekian and Satterlie, 2001).

Melibe leonina is the only lateral-bending swimming mollusc that has been investigated at the neural level. Given our current state of understanding, it appears as if the neural circuit for swimming in Melibe has some similarities, in terms of the overall organization, to the circuit used by the dorsal-ventral swimmers, such as Tritonia and Pleurobranchaea. First, the motoneurons play little, if any, role in producing the swim pattern. Second, most of the motoneurons are located in the pedal ganglia, although they are segregated in a different manner for side-to-side vs. dorsal-ventral locomotion. Third, reciprocal inhibition is a critical element involved in generating the alternating pattern of movement. Finally, some of the key interneurons are located in approximately the same location in all three species (see Katz et al. [2001] for more on this issue). However, a very key interneuron in Melibe resides in the pedal ganglion, as is the case in both of the parapodial flappers, Aplysia and Clione (Satterlie, 1985; Gamkrelidze et al., 1995), but neither of the dorsal-ventral swimmers. In the future, knowledge about the neural basis of swimming in some additional lateral-bending species, such as Dendronotus festivus, would be very helpful in determining the relative importance of mode of swimming vs. phylogenetic relationships in shaping the neural circuits underlying swimming.

The putative role of nitric oxide in Melibe swimming

Nitric oxide synthase has been identified in all of the species discussed in this Symposium (Moroz and Gillette, 1996; Moroz et al., 1996; Satterlie, personal communication), except Aplysia brasiliana (although it is present in Aplysia californica [Jacklet and Gruhn, 1994]). However, in contrast with serotonin (see Norekian and Satterlie, 2001; Katz et al., 2001), the role of NO in opisthobranch swimming is poorly understood. In Melibe, diaphorase staining reveals a pair of neurons in the cerebropleural ganglion, as well as dense staining of the cerebral neuropil and neurons in the tentacles and associated ganglia. Immunocytochemical staining confirms the presence of NOS in the cerebropleural neurons. Application of NO-donors slows the swim pattern from a rate of 1 cycle/2-5 sec, to 1 cycle/20-30 sec. These data, taken together with the known influence of NO on feeding in several molluscs (Moroz et al., 1993; Elphick et al., 1995; Teyke 1996), suggests a role of NO in feeding in Melibe. However, our results in studies with intact animals indicates that the slow pattern of activity induced by NO in pedal neurons is simply a very slow expression of the swim CPG. In intact animals, which are usually not swimming, this pharmacological effect of NO probably manifests itself as a reduction in the probability that animals will swim; which is also how both light and food influence swimming. Thus, our current hypothesis is that NO is involved in mediating either the inhibitory effects of light, or feeding stimuli, on the swim CPG.