Evidence that the Central Pattern Generator for Swimming in Tritonia Arose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior

Comparisons of the nervous systems of closely related invertebratespecies show that identified neurons tend to be highly conservedeven though the behaviors in which they participate vary. Allopisthobranch molluscs examined have a similar set of serotonin-immunoreactiveneurons located medially in the cerebral ganglion. In a smallnumber of species, these neurons have been physiologically andmorphologically identified. In the nudibranch, Tritonia diomedea,three of the neurons (the dorsal swim interneurons, DSIs) havebeen shown to be members of the central pattern generator (CPG)underlying dorsal/ventral swimming. The DSIs act as intrinsicneuromodulators, altering cellular and synaptic properties withinthe swim CPG circuit. Putative homologues of the DSIs have beenidentified in a number of other opisthobranchs. In the notaspid,Pleurobranchaea californica, the apparent DSI homologues (As1–3)play a similar role in the escape swim and they also have widespreadactions on other systems such as feeding and ciliary locomotion.In the gymnosomatid, Clione limacina, the presumed homologousneurons (Cr-SP) are not part of the swimming pattern generator,which is located in the pedal ganglia, but act as extrinsicmodulators, responding to noxious stimuli and increasing thefrequency of the swim motor program. Putative homologous neuronsare also present in non-swimming species such as the anaspid,Aplysia californica, where at least one of the cerebral serotonergicneurons, CC3 (CB-1), evokes neuromodulatory actions in responseto noxious stimuli. Thus, the CPG circuit in Tritonia appearsto have evolved from the interconnections of neurons that arecommon to other opisthobranchs where they participate in arousalto noxious stimuli but are not rhythmically active.     

Properties of central motor neurons exciting locomotory cilia inTritonia diomedea

Summary A pair of large, identifiable neurons (Pd 21), one in each pedal ganglion, can excite previously inactive locomotory cilia on the sole of the foot ofTritonia diomedea (Audesirk, 1978; Fig. 3). These neurons exert their effect via axons which innervate the foot and are probably central motor neurons for pedal cilia. IntactTritonia are stimulated to crawl by the application of 1.5 M NaCl to the tail, and conversely usually stop crawling when the chemosensitive oral veil is touched with food (sea whip,Virgularia sp.). The Pd 21 neurons are excited by 1.5 M NaCl applied externally to the tail, and are inhibited by sea whip touch to the oral veil (Figs. 4 and 5). When aTritonia performs its escape swim, the cilia move strongly, and the Pd 21 neurons fire bursts of spikes in phase with dorsal flexions (Figs. 6 and 7). After a swim, aTritonia rapidly crawls along the substrate; during this time the spiking rate of the Pd 21s is greatly accelerated. Interneurons thought to drive swim bursts produce monosynaptic EPSPs in the Pd 21s (Fig. 8). The Pd 21s are coordinated in their spike activity by synaptic activity which is synchronous in the two neurons regardless of the site of external stimulation, and by electrical coupling between the two cells via axons in a pedal commissure (Figs. 9 and 10). The coupling coefficient for passively conducted potentials is quite high, about 0.15, despite an axon 8 to 12 mm long separating the two cells.Abbreviations BPSP biphasic postsynaptic potential - SW sea water     

About possible functional interaction between serotonin and neuropeptides in control processes of embryogenesis (Experiments on embryos ofTritonia diomedea)

Ritanserin and inmecarb hydrochloride, antagonists of serotonin, act cytostatically and teratogenically on early embryos ofTritonia diomedea, a nudibranch mollusk. On the basis of a pharmacological analysis and the type of developmental abnormalities observed, this action appears to be due to disturbances in the functional activity of endogenous serotonin and is associated with damage to the cytoskeleton. The effects of ritanserin and inmecarb are prevented or attenuated by lipophilic serotonin analogs (serotoninamides of polyenoic fatty acids), as well as by polypeptides isolated from neurons Pd5 and Pd6 of the pedal ganglia of the adultTritonia. In late embryos (stage of veligers), serotonin and to a lesser extent its lipophilic analogs strongly increase embryonic motility. This effect of serotonin is potentiated by some neuropeptides and inhibited by others. These results provide evidence for functional interaction between serotonin and neuropeptides in the control processes of embryogenesis.     

Pedal neuron 3 serves a significant role in effecting turning during crawling by the marine slug <Emphasis Type="Italic">Tritonia diomedea</Emphasis> (Bergh)

The marine nudibranch Tritonia diomedea crawls using its ciliated foot surface as the sole means of propulsion. Turning while crawling involves raising a small portion of the lateral foot margin on the side of the turn. The cilia in the lifted area no longer contribute to propulsion, and this asymmetry in thrust turns the animal towards the lifted side. Neurons located in the pedal ganglia of the brain contribute to these foot margin contractions. T. diomedea has a natural tendency to turn upstream (rheotaxis), and pedal flexion neuron Pedal 3 elicits foot margin lift and receives modulatory input from flow receptors. To assess the contribution of this single cell in turning behavior, two fine wires were glued to the surface of the brain over left and right Pedal 3. We determined that Pedal 3 activity is correlated with subsequent ipsilateral turns, preceding the lift of the foot margin and the change in orientation by a consistent interval. Both Pedal 3 cells show synchronous bursts of activity, and the firing frequency of the ipsilateral Pedal 3 increased before turns were observed to that side. Stimulation of the electrode over Pedal 3 proved sufficient to elicit an ipsilateral turn in Tritonia.