Anomalous anatomy of identified neurons in the larval prawn: spontaneous and induced by microlesions

Abstract

The abdominal ganglia of the prawn Macrobrachium rosenbergii undergo developmental changes of fundamental interest between the time of hatching and metamorphosis. These changes include an increase in cell numbers and changes in the connectivity between identified neurons. The giant motoneurons involved in the escape response, which form a syncytium in the adult, are observed as separate neurons with crossed axons in early larvae.Anomalous growth and connections of identified neurons were studied in order to gain some understanding of the rules and mechanisms governing normal development. Spontaneous anomalies included: supernumerary axons and abnormal axonal trajectories. The plasticity and specificity of identified neurons were studied by following the anatomical effects of deletions of giant neurons. Microlesions were inflicted reproducibly by means of a focused beam of visible and ultraviolet light. Within a day, irradiated cell bodies are eliminated; complete disappearance of the axon takes about 10 days, indicating that the remarkable ability of some invertebrate neurons to survive without a soma is not present in the larval prawn. As a result of the removal of an axon, the most common effect found in central connections was the absence of the collaterals or axons deprived of their targets. No collateral sprouting was detected in the central nervous system. In about a third of the ganglia where a giant motoneuron was killed and structure was analyzed 2 or more weeks after irradiation, anomalous connections were found. They usually involved contacts between an interneuron deprived of its normal target and the contralateral motoneuron which remained intact. The restricted types of anomalies observed support the notion of a hierarchical order in the rules governing formation of central synapses, in which neuron type ranks higher than laterality.Decapod crustaceans, such as crayfish and lobsters, have been animals of choice of neurobiologists for many years. The main reason for this is their relatively simple nervous system; the fact that several of their cells are remarkably large and can be identified according to a variety of anatomical and physiological criteria is also a contributing factor in their choice. The giant Malaysian prawn, Macrobrachium rosenbergii, shares the advan-' This work was supported by National Institutes of Health Grants NS 09821 and RR-00442.We thank D. Soroker and M. Spira for kindly letting us know details of their unpublished observations on the connectivity of the giant fibers of the adult prawn. We also thank A. F.

Motor neurons in the escape response circuit of white shrimp (Litopenaeus setiferus)

“…Although the size and hypothesized fusion in the MoG cell body is unexpected, it is consistent with the long-known fusion of the MoG axons in other caridean shrimp species ( Johnson, 1924 ; Holmes, 1942 ; Friedlander & Levinthal, 1982 ). Given that there are genetic mechanisms to fuse the MoG axons during development ( Friedlander & Levinthal, 1982 ), the same mechanisms could be used to fuse cell bodies.…”

“…Although the size and hypothesized fusion in the MoG cell body is unexpected, it is consistent with the long-known fusion of the MoG axons in other caridean shrimp species ( Johnson, 1924 ; Holmes, 1942 ; Friedlander & Levinthal, 1982 ). Given that there are genetic mechanisms to fuse the MoG axons during development ( Friedlander & Levinthal, 1982 ), the same mechanisms could be used to fuse cell bodies. Reduction of fusion appears to be an evolutionary trend in the decapods, starting with hypothesized fusion of MoG cell bodies (this study) and axons in dendrobranchiates (this study; Xu & Terakawa, 1999 ), to fusion of the MoG axons only in carideans ( Holmes, 1942 ), to no MoG fusion in reptantians ( Mittenthal & Wine, 1978 ).…”

“…Because of the combination of giant interneurons and myelin, shrimp giant axons have the fastest conduction velocity known ( Xu & Terakawa, 1999 ). Second, the left and right fast flexor motor giant neurons (MoGs) are separate in crayfish ( Mittenthal & Wine, 1978 ), but the MoG axons fuse in caridean shrimp and prawns ( Johnson, 1924 ; Holmes, 1942 ; Friedlander & Levinthal, 1982 ). Axonal fusion may promote greater synchrony in muscle activation, which should in turn lead to more powerful tailflips.…”

Bilateral branching contributes minimally to the enhanced ipsilateral projection in monocular Syrian golden hamsters

“…It is difficult to envision how laterality could confer on a cell its particular properties, since there is no evidence that cells behave differently on one side of the brain versus the other. Studies of the synaptic patterns of anomalously crossed projections in hamsters (Finlay et al, 1979) and prawns (Friedlander and Levinthal, 1982), for example, suggest that when cells err in laterality, they maintain their original specificity of synaptic connectivity. Therefore, rather than suppose that laterality confers to a cell its particular properties, it seems more likely that a fiber is in some fashion pre-committed along with other characteristics to its particular laterality.…”