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AMER. ZOOL., 41:939–942 (2001) Swimming in Opisthobranch Mollusks: Contributions to Control of Motor Behavior: Introduction to the Symposium1 RICHARD A. SATTERLIE2 Department of Biology, Arizona State University, Tempe, Arizona 85287-1502 Beginning with the pioneering work of Dennis Willows (Willows and Hoyle, 1969; Willows et al., 1973), studies utilizing opisthobranch mollusks have been particularly useful in the description of rhythmic motor behaviors and their mechanisms of central pattern generation. General mechanisms that contribute to central pattern generator function in other animal groups, such as reciprocal inhibition, postinhibitory rebound, multi-component synaptic potentials, delayed excitation, and extrinsic modulation (to name a few), have been found to contribute to the generation of rhythmic motor behavior in opisthobranchs. In addition, some novel concepts that have since been substantiated in other animal groups were developed through work on opisthobranch locomotory systems: some CPG neurons are multifunctional and may participate in different motor behaviors (Getting, 1989); networks can be intrinsically modulated by components within the CPG networks (Katz et al., 1994; Katz and Frost, 1995). The Opisthobranch Swimming symposium was organized with a primary goal of providing details of motor control from four specific Opisthobranch orders that have swimming members. This comparative approach is particularly interesting since behavioral observations of swimming activity in the four orders reveal three distinct types of swimming. In the Anaspids (Aplysia) and Gymnosomes (Clione), swimming is accomplished by flapping of parapodia. In the latter group, parapodia are highly modified into wings. In the Notaspids (Pleurobranchaea) and dorso-ventrally flattened Nudibranchs (Tritonia), swimming consists of 1 From the Symposium on Swimming in Opisthobranch Mollusks: Contributions to Control of Motor Behavior presented at the Annual Meeting of the Society for integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia. 2 E-mail: [email protected] alternate dorsal and ventral flexions of the body. Finally, in the laterally flattened Nudibranchs (Melibe), swimming occurs with alternating lateral flexions of the body. In all but one case (Clione), the central neural circuits and effectors for swimming also participate in other behaviors. For example, the parapodia of Aplysia undergo local protective contractions in response to directed stimulation and produce coordinated respiratory pumping contractions in addition to their role in swimming (Kandel, 1979). In the Notaspids and Nudibranchs, the effectors and at least some of the central circuitry underlying effector activity are involved in local retraction movements and local bending responses in addition to swimming contractions. A comparative look at the polymorphic nature of the neuromuscular systems of these animals is thus of interest. Clione is unusual in that the central circuitry and peripheral musculature used in swimming appears to be dedicated to that behavior. Despite this, many features of the Clione swim control system appear to be similar to that of Aplysia. Using this as one example, a secondary goal of the symposium was to allow some speculation on inter-order relationships based on common and unique properties of the neural machinery that generates these different forms of swimming. An additional objective of the symposium was to honor Dr. A. O. Dennis Willows for his groundbreaking work on the Tritonia swimming system (Willows and Hoyle, 1969; Willows et al., 1973). The symposium participants are either Dennis’s academic children, grandchildren, or ‘‘adopted brothers/nephews,’’ and all have benefited from his help and encouragement through his roles of colleague and collaborator, and as Director of the Friday Harbor Laboratories of the University of Washington. The following symposium papers bear 939 940 RICHARD A. SATTERLIE a direct stamp of Dennis’s work on, and interest in, Opisthobranch swimming. The list of participants of this symposium is short two important contributors whose research careers were tragically cut short. This symposium acknowledges the important contributions of Drs. Peter Getting and Harold Pinsker, whose seminal investigations have molded our current work, not only with respect to swimming in Tritonia (Getting) and Aplysia (Pinsker), but also well beyond work on swimming Mollusks. One common theme that emerged from the symposium that deserves discussion here is the role of serotonin in modulating swimming activity in all five opisthobranchs (Aplysia, Clione, Melibe, Pleurobranchaea and Tritonia). Serotonergic modulation of locomotion is a well-known feature of a wide variety of animals, including vertebrate spinal locomotory circuits, in which serotonin has been shown not only to enhance muscle tone to produce an increase in locomotor activity (e.g., Barbeau and Rossignol, 1991), but also to initiate locomotor activity (Crowley and Schmidt, 1994; Sillar and Simmers, 1994; Gerin et al., 1995). In mammals, serotonin has been shown to initiate locomotion in decerebrated, curarized rabbits (Viala and Buser, 1969), and in neonatal rats (Cazalets et al., 1992; Cazalets, 1995). In more than one symposium presentation, modulatory cells were considered to comprise a general serotonergic arousal system that was capable of up-modulating swimming, as well as other non-swimming activities. This highlights a need for a brief discussion of putative properties of such general arousal systems. The following is meant to be a starting point for further thought and discussion on the concept of ‘‘arousal,’’ particularly when the following papers from this symposium are read. Many of the following points were adapted and modified from Kandel (1979), Teyke et al. (1990), and Kupfermann et al. (1991). First, the concept of arousal, as presented here, is distinct from motivational variables that produce specific goal-oriented behavior, such as those that serve to correct or satisfy a well-defined physiological or homeostatic imbalance/need (e.g., feeding, thirst). The latter would be better termed a ‘‘motivational state’’ (Kandel, 1979). The distinction between a motivational state and an arousal may involve different ‘‘levels’’ within a modulatory hierarchy since an arousal system may be activated as part of an overall motivational state. This leads to a second property of arousal systems: they may be activated, in whole or in part, during more than one type of behavior. Whereas a motivational state is directed towards one primary goal, an arousal system may function as a general gain setting system that is utilized in a variety of different behaviors. As a specific example, swim acceleration in the pteropod mollusk Clione, which is triggered by activity in a serotonergic ‘‘arousal’’ system, is used during several different behaviors: avoidance behavior, startle-related escape, acquisition and comsummatory phases of feeding behavior, and at the conclusion of egg laying (to break the animal away from the egg mass). While both motivational and arousal states would alter activity in lower levels of the motor system through excitatory, permissive, or inhibitory influences, arousal systems would be multifunctional, while motivational states would be dedicated to a specific goal. In addition, the multifunctional nature of arousal systems should place them at a lower hierarchical level than motivational states, which may include activation of an arousal system as part of the overall response. Motivational and arousal states produce modulatory effects that typically persist for some time after cessation of the initiating stimulus. While motivational states can last for fairly long periods (minutes/hours), the arousal responses of opisthobranchs, reported in the following papers, typically are of much shorter duration. This raises a pair of interesting questions. Are specific cells involved in the maintenance of long duration motivational states, and if so, are they separate from cells involved in the initiation of motivation? The likelihood of positive answers to these questions is higher for motivational states than for arousal systems provided the former are directed to correction/satisfaction of a physiological need. The modulatory action of at least some of OPISTHOBRANCH SWIMMING the serotonergic arousal systems of opisthobranchs appears to operate via second messenger systems, and their time course is limited by the activation/deactivation parameters of these cellular responses. Furthermore, as an example, the time course of swim acceleration in Clione is limited by the duration of activation in two clusters of cerebral modulatory neurons, plus a 5–10 sec period following cessation of spike activity (Satterlie and Norekian, 1995). The ability of modulatory states to organize a variety of neuronal circuits presents a potentially interesting difference, when motivational and arousal states are compared. The influence of motivational states should be widespread, involving activity in several independent circuits. While the suite of circuits can vary with the type of stimulus, overall, there should be some consistency imposed on such a system since the motivational state is designed to address a specific physiological need. On the other hand, arousal systems presumably subserve several different behaviors and should show significant flexibility to mesh with the specific needs of each behavior. As an example, the serotonergic system of Clione appears to be compartmentally organized. Individual, or small groups, of serotonergic cells modulate specific effectors, such as the heart and swimming musculature. While each ‘‘compartment’’ can operate independently, they are activated together to produce a full suite of physiological responses during swim acceleration (Satterlie and Norekian, 1995). Potentially, different combinations of modulatory cells could also be simultaneously activated during different behaviors, imposing a polymorphic nature on the modulatory arousal system. In this, and several of the following papers, reference is made to ‘‘serotonergic arousal systems.’’ While the cells/circuits that modulate swimming in these opisthobranchs utilize serotonin, this does not imply that these and other arousal systems are transmitter specific. The possibility of release of multiple neuroactive substances from single neurons presents a potential source of variability in modulatory systems, as does the potential participation of neurons with different transmitter phenotypes. 941 In the following set of papers, an initial attempt was made to group papers according to opisthobranch species, so the reader would be familiar with the peculiarities of each animal when reading multiple papers describing work on a single species. This was abandoned in favor of a more topical organization, although an attempt was made to group papers by species when possible. It is hoped that the symposium papers will stimulate further interest in the comparative analysis of motor control, and highlight the value of invertebrate preparations in this enterprise. ACKNOWLEDGMENTS I would like to thank the symposium participants for their efforts in producing the oral presentations and written works. The symposium was generously supported by the National Science Foundation (IBN 9905990)—special thanks to Dr. Elvira Doman, Program Officer of the Integrative Animal Biology Program. We are also grateful to the Division of Neurobiology of the Society for Integrative and Comparative Biology for financial support, and Dr. Paul Katz and Georgia State University for organizing a social gathering during the meeting. REFERENCES Barbeau, H. and S. Rossignol. 1991. Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs. Brain Res 546:250–260. Cazalets, J. R. 1995. Dual control of central pattern generators: Neonatal rat spinal cord in vitro. In W. R. Ferrell and U. Proske (eds.), Neural control of movement, pp. 187–194. Plenum, New York. Cazalets, J. R., Y. Sqalli-Houssaini, and R. Clarac. 1992. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J. Physiol. 455:187–204. Cowley, K. C. and B. J. Schmidt. 1994. A comparison of motor patterns induced by N-methyl-D-aspartate, acetylcholine, and serotonin in the in vitro rat spinal cord. Neurosci. Lett. 171:147–150. Gerin, C., D. Becquet, and A. Privat. 1995. Direct evidence for the link between monoaminergic descending pathways and motor activity. I. A study with microdialysis probes implanted in the ventral funiculus of the spinal cord. Brain Res. 704:191– 201. Getting, P. A. 1989. Emerging principles governing the operation of neural networks. Ann. Rev. Neurosci. 12:185–204. 942 RICHARD A. SATTERLIE Kandel E. R. 1979. Behavioral biology of aplysia, pp. 351–371. W. H. Freeman, San Francisco. Katz, P. S. and W. N. Frost. 1995. Intrinsic neuromodulation in the Tritonia swim CPG: The serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2. J. Neurosci. 15:6035–6045. Katz, P. S., P. A. Getting, and W. N. Frost. 1994. 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