Development of Locomotor Patterns in the Absence of Peripheral Sense Organs and Muscles

Abstract

The role of peripheral sense organs and muscles in specifying the circuitry of the central nervous system during ontogeny was tested in larval lobsters. Presumptive locomotor appendages, the abdominal swimmerets, were extirpated before their differentiation. Electrophysiological recordings made 2-4 weeks later from the corresponding motor nerves showed that, despite the absence of the target muscles and sense organs, normal reflexes and normal patterns of rhythmic locomotor output appeared in the swimmeret motoneurons at the usual developmental stage. Therefore, target muscles and sense organs are unnecessary to the differentiation of normal motor output patterns in this simple invertebrate locomotor system.The role of the periphery in determining the circuitry of the central nervous system has been studied and debated for nearly a century (1-5). According to one view, peripheral sense organs and muscles provide the central nervous system with essential information for specifying and modifying synaptic connections. Sensory feedback from movements in a developing motor system, for example, could help organize the corresponding central connections. Similarly, a muscle could, in principle, "instruct" its motoneurons to form appropriate central connections by means of biochemical "messages" conveyed centrally from the muscle-the well-known hypothesis of myotypic specification. Such hypotheses are significant not only for ontogeny and regeneration, but also for neuronal plasticity in general; if the periphery can indeed influence central circuitry, the underlying mechanisms could have implications for theories of learning and memory.Evidence on the role of the periphery in establishing central circuitry consists largely of behavioral observations (3). Such evidence suggests that in some motor systems, at least, sensory input or feedback may not be necessary to the formation of normal movements during development (6-11) or after limb transplantation (12). Decisive tests using electrophysiological methods, however, are lacking. Myotypic specification seemed an attractive explanation for transplantation data (12-14), but more recent studies support alternative mechanisms (4, 15-17), and in any case a possible ontogenetic role for myotypic specification has not been studied previously.The present study was undertaken to test the role of peripheral structures in specifying central nervous connections during the ontogeny of a simple locomotor system, the abdominal swimmerets of the lobster. This motor system was chosen because its neuronal organization is well understood in adults (18-29) and because it develops largely after larvae hatch from the egg (5, 30, 31). Swimmeret sense organs and muscles are undifferentiated at hatching, but the appendages are fully developed and capable of rhythmic locomotor movements 3 weeks later, when the larvae molt to the fourth larval stage (5). Thus it was possible to interfere with the normal developmental sequence by extirpation of presumptive swimmeret tissue, and to examine t...

The structure and function of thoracic exopodites in the larvae of the lobster Homarus gammarus (L.)

“…Similar developmental questions are posed by the other behaviour patterns which appear for the first time in stage IV. The ontogeny of the swimmeret system has been studied by Davis (Davis 1973;Davis & Davis 1973), and its particular relation to larval exopodite beating is considered in the present study . Also is strikingly different in larval and post-larval lobsters (figure 8) and it may be possible to interpret this difference in terms of the developing action of the various types of motor element which have been shown to control tail flexion in the adult Macrura (Bowerman & Larimer 1974;Larimer, Eggleston, Masukawa & Kennedy 1971;Schrameck 1970;Wiersma 1938;Wine & Krasne 1972).…”

Sensory deprivation during development decreases the responsiveness of cricket giant interneurones

“…It has been demonstrated that motor neurone firing patterns for cricket song (Bentley & Hoy, 1974) lobster swimmerett beating (Davis, 1973) and locust flight (Kutsch, 1974) develop normally in the absence of sensory feed-back. These results combined with the well known stereotypy of behaviour among invertebrates and the demonstration of genetic control of motoneurone firing patterns (Bentley & Hoy, 1974) have supported the view that the development of normal function in the invertebrate nervous system is independent of experience.…”

A quantitative analysis of exopodite beating in the larvae of the lobster Homarus gammarus (L.)

“…The study is intrinsically interesting as an analysis of a swimming behaviour in an animal with a relatively rigid body that locomotes by beating appendages serially. Because the analysis was conducted on a developing system through several stages it provides new information about behavioural development and, in association with previous work (Davis 1973(Davis , 1974Davis & Davis 1973), poses further questions in that area. The developmental aspect of the study is dealt with further in the third paper .…”

“…In the lobster, H o m a m s, it has also proved possible to examine swimmeret beating activ in the early developmental stages (Davis 1974), and Davis and his colleagues have produced evidence that the motor patterning responsible for swimmeret beating, which appears first in stage IV of development, is present in the central abdominal ganglia in the absence of prior sensory input from the swimmerets (Davis 1973;Davis & Davis 1973). Although swimmeret beating does not start until stage IV, it is not the first rhythmic activity of the larva.…”

“…Although the argument presented is hypothetical and based on descriptive similarities which might well be fortuitous, it is worthy of consideration because of the changes found in larval development (Laverack et al 1976) and also because of results sugg lobster oscillators develop in the absence of sensory input but are subsequently modified by it (Davis 1973(Davis , 1974Davis & Davis 1973).…”