The Telson Flexor Neuromuscular System of the Crayfish I

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The Telson Flexor Neuromuscular System of the Crayfish I J. exp. Biol. 127, 249-277 (1987) 249 Printed in Great Britain © The Company of Biologists Limited 1987 THE TELSON FLEXOR NEUROMUSCULAR SYSTEM OF THE CRAYFISH I. HOMOLOGY WITH THE FAST FLEXOR SYSTEM BY J. P. C. DUMONT* AND J. J. WINE Department of Biological Sciences and Department of Psychology, Stanford University, Stanford, CA 94305, USA Accepted 26 June 1986 SUMMARY 1. We describe the phasic neuromuscular system of the crayfish telson and establish its homology with the abdominal flexor system that provides the power- stroke for tailflip escape responses. 2. Three paired phasic telson muscles are innervated by 11 paired neurones which have somata in the terminal (sixth) ganglion and axons in the sixth nerve. These are the posterior and ventral telson flexors and the anterior telson muscle. 3. Studies of embryonic ganglia provide evidence that the sixth ganglion is a fusion product of two ancestral ganglia, plus a partial ganglion that is not homologous with the segmental ganglia. 4. Two of the telson flexor motor neurones are homologues of the single motor giant found in each anterior hemiganglion. Among the shared features which led to this conclusion are: size, soma position, distribution of terminals to the muscles, dendrite morphology, pattern of direct inputs from the giant axons, and the marked tendency for low-frequency depression of the neuromuscular synapse. 5. Two of the telson flexor neurones are homologues of the single flexor inhibitor found in each anterior hemiganglion. In addition to numerous morphological similarities, these two cells produce IPSPs in the telson flexor muscles. 6. Six of the seven remaining motor neurones were identified as homologues of the non-giant fast flexor excitors of anterior ganglia. These can be divided into two uneven groups according to their ganglia of origin. The sixth segmental group of fast flexor motor neurones consists of four neurones (one less than expected) and the seventh segmental group consists of two neurones (three less than expected). 7. The remaining neurone provides the sole innervation of the anterior telson muscle. Although previously classified as a telson flexor muscle, we found that the anterior telson muscle moves the uropod but not the telson. The innervation of this muscle and the pattern of inputs to the anterior telson motor neurone from identified interneurones are unlike that of any fast flexor muscle or motor neurone. We conclude that the anterior telson muscle and its motor neurone are not homologues of anterior components of the fast flexor system. •Present address: Faculty of Medicine, McGill University, Montreal, Quebec, Canada. Key words: evolution, homology, neurones, invertebrate. 250 J. P. C. DUMONT AND J. J. WlNE 8. In anterior ganglia, a prominent premotor neurone known as the segmental giant is presynaptic to all fast flexor motor neurones except the motor giants and flexor inhibitors. We identified a single paired cell in the sixth ganglion which appears to be the segmental giant homologue. INTRODUCTION In this paper we describe a neuromuscular system in the tailfan of the crayfish and establish its homology with the neuromuscular systems that provide the flexion powerstroke for tailflip escape responses. This is intended to provide the basis for an examination of the alteration of these circuits during their evolution. More specifi- cally, by improving our understanding of crayfish escape circuitry, and extending it to include the tailfan, we hope to be able to decide whether specific components of these circuits are the result of selection of adaptive features or are due to the influence of non-adaptive evolutionary determinants such as developmental constraints (see Gould & Lewontin, 1979). Our study takes advantage of the considerable amount of existing data on the organization of crayfish escape behaviour (see below), and of a key feature of arthropod and annelid evolution: the differential modification of repeated body segments within and across species. These differences provide an opportunity to make intersegmental comparisons within a single species among serially homologous neural circuits, with the aim of documenting differences in the structure and function of identified, homologous neurones. Within one animal, adjacent segments in a given compartment (such as two mid-abdominal ganglia in a crayfish) are very similar, so that it is relatively easy to establish homologies and to detect subtle differences between the segments. More widely separated or specialized ganglia within the same compartment (such as the mid-abdominal and terminal ganglia of crayfish), while appearing quite dissimilar on direct comparison, may be homolo- gized by a stepwise comparison via the intervening ganglia. Ganglia in different compartments, such as thoracic and abdominal ganglia in crayfish, may be so different that homologies cannot be established without developmental data (see Bate, Goodman & Spitzer, 1981). However, even in highly dissimilar ganglia some features are usually conserved and can serve to orientate the investigator. The fast flexor system of the crayfish abdomen is well suited for both inter- segmental and interspecific comparisons. The abdomen consists of five similar segments and a highly specialized terminal segment, the tailfan. The fast flexor system, which mediates the powerstroke of the crayfish tailflip escape response, has been studied extensively (Takeda & Kennedy, 1964; Kennedy & Takeda, 1965; Mittenthal & Wine, 1973, 1978; Miller, Hagiwara & Wine, 1985). The neuro- muscular system of the tailfan has also been studied previously (Larimer & Kennedy, 1969; Larimer, Eggleston, Masukawa.& Kennedy, 1971; Kramer, Krasne & Wine, 1981) but none of the studies of the tailfan include identification of the motoo neurones, or more than tentative establishment of homology. Segmentally homologous neurones in the crayfish I 251 The fast flexor escape system exists in a wide range of modern species. For example, it appears to be homologous in crayfish and the syncarid crustacean, Anaspides tasmaniae (Silvey & Wilson, 1979), which diverged about 300 million years ago. The telson flexor neuromuscular system is an especially good subject for comparative study because systems that are presumably homologous have been described in other decapod Crustacea (Paul, 1981; Paul, Then & Magnuson, 1985). Additional and more parochial interest in the telson system arises from a con- troversy about whether the system is a fusion product of two ancestral segments. Johnson (1924) proposed that the sixth abdominal ganglion (G6) is a fusion product, because of the presence of two lateral giant (LG) segments (see also Kondoh & Hisada, 1983) and two motor giant neurones (MoGs) in this hemiganglion, as opposed to one of each in other abdominal hemiganglia. However, Johnson's identifications were based solely on morphology. Larimer & Kennedy (1969), using physiological techniques, proposed that only 10 phasic motor neurones innervate the telson flexors, including only a single peripheral inhibitor. Since their count matched earlier counts of fast flexor axons in the flexor motor nerve of ganglion 3, and since they found rio evidence for either an extra MoG or LG segment, they concluded that the evidence for fusion was not convincing. The issue of fusion is important because, if it did occur, it must have been accompanied by considerable reorganization if we are to account for the doubling of some neurones with no increase in the total number of efferents. Our task was made easier by recent research which has made it clear that the fast flexor system is not composed of a segmentally iterated series of identical ganglionic networks. Intersegmental differences have been found in the number of motor neurones (Mittenthal & Wine, 1978), the number of interneurones (Kramer et al. 1981), and the presence (Mittenthal & Wine, 1973) or strength (Miller et al. 1985) of synaptic connections. Both segmental and intersegmental neurones have been found interposed between fast flexor motor neurones and the giant command neurones that had previously been thought to fire them directly (Kramer et al. 1981; Roberts et al. 1982). Major intersegmental differences have been found in various fast flexor pathways (Mittenthal & Wine, 1973; Miller et al. 1985). In this respect, the sixth ganglion appears to be particularly specialized (Kramer et al. 1981), and therefore worth further examination. In this paper we present the evidence for homology between the telson flexor neuromuscular system and the fast flexor system of anterior ganglia. In the following papers (Dumont & Wine, 1986a,6), we examine the differences between the fast flexor pathways of the anterior segments and the telson. MATERIALS AND METHODS Crayfish, Procambarus clarkii, were purchased from a variety of commercial Suppliers and kept in communal tanks. 252 J. P. C. DUMONT AND J. J. WlNE Cobalt backfills The telson motor neurones were backfilled with cobaltous chloride (Pitman, Tweedle & Cohen, 1972) using nerve cords isolated from the last three segments of the abdomen (see below). When a cut sixth nerve was immersed in cobaltous chloride solution (2-5 moll"1) for 9h, only the large, phasic telson motor neurones were filled. If a nerve was immersed overnight, the tonic motor neurones were also filled. The cobalt was then precipitated with a few drops of ammonium sulphide. To identify the innervation of particular muscles, individual branches of the sixth nerve were backfilled. The branches innervating the dorsal
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