Locomotion in Aplysia: triggering by serotonin and modulation by bag cell extract

Locomotion in Aplysia is mediated by a central program. We have found that this program is triggered by the biogenic amine, serotonin (5HT), and modulated by an endogenous source of neuropeptides, bag cell extract. In examining the triggering of locomotion, we found that injecting 5-HT into the bloodstream of quiescent animals elicited locomotion in both intact, freely moving animals and split-foot preparations. Increasing the concentration of 5-HT from lop7 to lop3 M produced both a monotonic increase in the number of steps elicited over a 5-min period after injection and a monotonic decrease in the first interstep interval. The threshold for triggering locomotion was lop7 M in split-foot preparations. Application of a saturated salt solution to the tail-a natural trigger for escape locomotionfacilitated 5-HT locomotion. The effects of 5-HT on locomotion were relatively specific since they were not mimicked by three other biogenic amines known to exist in Aplysia (dopamine, octopamine, and histamine). 5-HT could still trigger locomotion after isolating the pedal and pleural ganglia from the rest of the central nervous system, suggesting that a primary site for the action of 5-HT on locomotion lies in the pedal and pleural ganglia. In examining the modulation of locomotion, we found that injecting bag cell extract, an endogenous source of neuropeptides in Aplysia which elicits egg-laying behavior, reversibly suppressed 5-HTtriggered locomotion. As in the case with serotonin, bag cell extract suppression of locomotion was still observed in animals in which the pleural and pedal ganglia were isolated from the rest of the central nervous system. The suppression of locomotion was specific to bag cell extract since no suppression was produced by extracts of other central nervous tissue (cerebral ganglia). Moreover, the suppressive effect of bag cell extract was abolished by prior treatment of the extract with pronase, suggesting that the active suppressive agent is one or more of the peptides specific to the bag cells. Thus, locomotion in Aplysia provides a useful model system for examining both the triggering and the modulation of a fixed action pattern. Locomotion in Aplysia californica is a centrally programmed behavioral sequence which is utilized by the animal to accomplish a number of different behavioral objectives. Thus it is integrated with many other components of the animal’s behavioral repertory. As a result, locomotion can be elicited and modulated by a variety of ’ This work was supported by National Institute of Neurological and Communicative Disorders and Stroke Grant NS12744, a Schepp Foundation Scholarship to S. M. , and Career Development Award MH 0081 to T. J. C. We wish to thank E. R. Kandel for his many helpful discussions and for his useful criticisms of an earlier draft of the manuscript, U. Koch and J. Koester for their assistance in the in uivo preparations, and K. Weiss for his suggestions concerning pronase treatment of bag cell extract. * To whom correspondence should be addressed, at Center for Neurobiology and Behavior, New York State Psychiatric Institute-Annex, 722 West 168 Street, New York, NY 10032. factors including appetitive stimuli (Preston and Lee, 1973; Kupfermann, 1974; Advokat et al., 1978), noxious stimuli (Wachtel and Impelman, 1973; Walters et al., 1978), reproductive behavior (Strumwasser et al., 1969, 1980; Arch, 1976), and both nonassociative and associative learning (Walters et al., 1979, 1981). Moreover, locomotion in Aplysia is well suited for a cellular analysis (Jahan-Par-war and Fredman, 1978a, b, c; Henning et al., 1979). Thus, this fixed action pattern is an excellent system to explore the neural mechanisms involved in the triggering and modulation of a complex behavior. As a first step in this direction, we have examined the triggering effects of several biogenic amines and the modulating effects of bag cell extract (BCE), which contains at least four neuropeptides, including egg-laying hormone (Loh et al., 1975; Arch et al., 1976a, b; Stuart et al., 1980; Scheller et al., 1982). We found that micromolar injec-