Understanding the neural mechanisms that underlie the evolution of species-specific behavior is a fundamental quest in biology. This project takes advantage of unique characteristics of the nervous systems of gastropod molluscs (sea slugs) that allow detailed comparisons to be made of the neuronal circuits underlying behavior in closely-related species. In sea slugs, distinct nerve cells or neurons can be recognized among individual animals within a species based on unique anatomical and physiological characteristics. The same characteristics can be used to recognize those neurons in the brains of other sea slug species. In this way, the roles of these neurons in producing behavior can be assessed. The project uses electrophysiological and neuroanatomical techniques to study the properties of neurons and their connections. It also uses new techniques for probing the genes that are expressed by individual neurons. The project uses a new web-based tool called NeuronBank.org to allow students and researchers at several institutions to share results of research projects. This will provide a training opportunity for students to learn basic neurobiological techniques and apply them to an important scientific question. It is expected that uncovering the differences in simpler circuits in sea slugs will provide an understanding of how complex behaviors arose during evolution. Just as one would like to know how human intelligence arises from a brain structure that is similar to that of monkeys, sea slugs offer the opportunity to figure out how species can differ at the level of circuits composed of identified neurons, something that is currently not feasible to investigate in mammals.
There are over 2000 species of nudibranchs in the world's oceans. Yet fewer than 100 can swim. This project has been examining the nervous systems of these beautiful animals to understand the fundamental principles underlying how neural circuits produce behavior. More can be learned about fundamental principles by comparing two species than by studying a single species because if you don't compare, then you cannot determine which aspects of the circuit are fundamental and which are idiosyncratic to that species. Another reason for studying these sea slugs is that the swimming behaviors that they produce are quite simple, consisting of body flexions. Some species, such as Tritonia diomedea, swim by flexing their bodies up and down, while other species, such as Melibe leonina, swim by flexing side to side. The brains of these animals are relatively simple; they have a total of about 10,000 nerve cells (neurons). Fewer than ten of those neurons are directly involved in producing the swimming behavior. Finally, we can identify these neurons and recognize the same individual neurons in each species, so we can directly compare how a circuit in one species operates to how it operates in anothe species. We found that categorically different behaviors, dorsal-ventral (DV) swimming vs left-right (LR) swimming, are produced by different sets of neurons. Yet the homologues of neurons that produce DV swimming in Tritonia influence LR swimming. Those neurons use the neurotransmitter serotonin, which has important roles in all animals. We also found that in species that both produce DV swimming (Tritonia and a non-nudibranch, Pleurobranchea californica) the serotonin-containing neurons had the same effect. Furthermore, we found that a species that does not produce the DV swim lacks the serotonin effect. This indicates that this effect might be important for causing that swimming to occur. Another finding that we made is that even species that exhibit the same motor pattern can do it differently. The two sea slugs, Melibe leonina and Dendronotus iris both swim with side to side flexions. But in one species, a neuron called Si1 is part of the circuit and in the other species it is not. Thus, there are differences in how these circuits are put together. To summarize, we found that we could recognize the same neurons in many different species. How those neurons were assembled to produce swimming behaviors varied. This indicates that there are many different solutions to the same problem of swimming.
