Patterns of appearance of serotonin and proctolin immunoreactivities in the developing nervous system of the American lobster

Abstract

Serotonin (5-HT) and proctolin, neurohormones widely distributed in the lobster nervous system, have been implicated in a variety of behaviors and also are known to coexist in large pairs of identified neurons in the fifth thoracic (T5) and first abdominal ganglia (A1) of adults (Siwicki, Beltz, and Kravitz, 1987). Earlier studies also have shown that these paired neurons already contain 5-HT in embryos approximately halfway through development, whereas proctolin immunoreactivity does not appear in these cells until near the time of hatching (Beltz and Kravitz, 1987a). In the current studies, the brain and ventral nerve cord have been screened for the appearance of serotonin and proctolin immunoreactivities using immunocytochemical and biochemical methods, in order to determine whether the late appearance of proctolin in the paired T5 and A1 cells is a general feature of development in other neurons as well. In embryos approximately halfway through development, the adult complement of 5-HT-staining cells is already present. In several cases, embryonic serotonin cells are proportionally very large and prominent, suggesting possible developmental roles. In contrast to serotonin, fewer than 10% of the proctolin-staining neurons of juvenile animals are seen in embryos halfway through development. The number of immunoreactive cells gradually increases, but even by the sixth larval stage only half the number of cells that will eventually stain for proctolin are observed. Therefore, the developmental appearance of proctolin in lobster neurons, assayed using immunocytochemical methods, is relatively late and protracted compared to the appearance of serotonin. Quantitative measurements for 5-HT in lobster larvae were performed using high pressure liquid chromatography (HPLC) with dual electrochemical detection and for proctolin using radioimmunoassay. A gradual, probably growth-related increase in the amounts of serotonin and proctolin were seen during larval development. The implications of the biochemical data, in light of the immunocytochemical studies, are discussed.

Serotonin DepletionIn VivoInhibits the Branching of Olfactory Projection Neurons in the Lobster Deutocerebrum

“…The early appearance of serotonin during the development of both vertebrates (Lauder and Bloom, 1974;Fujimiya et al, 1986) and invertebrates (Taghert and Goodman, 1984;Glover et al, 1987;Goldberg and Kater, 1989;Beltz et al, 1990) has led to the hypothesis that this neurotransmitter plays an important role in the regulation of neural development (for review, see Whitaker-Azmitia et al, 1996;Levitt et al, 1997). This hypothesis has been supported by studies demonstrating that perturbations of serotonin levels can effect the development of neuropil areas that receive serotonergic innervation during development (Rhoades et al, 1993;Bennett-Clarke et al, 1994;Cases et al, 1996;Benton et al, 1997).…”

“…These neurons must then grow into the deutocerebral neuropils and intercalate into the existing neuronal circuits. The dense serotonergic innervation of the deutocerebral neuropils that is present during embryonic development also remains stable throughout the postembryonic development of the lobster (Beltz et al, 1990). Serotonin may therefore continue to play a role in regulating the morphogenesis of projection neurons throughout the lifetime of the animal.…”

Effects of proctolin on contractions, membrane resistance, and non- voltage-dependent sarcolemmal ion channels in crustacean muscle fibers

“…The penta-peptide proctolin (H-Arg-Tyr-Leu-Pro-Thr-NH,) was originally isolated as "gut-factor" from the cockroach Periplaneta americana (Brown, 1967). Subsequently, its presence was demonstrated in neurons of a number of arthropods, mainly crnstaceans and insects (e.g., Bishop et al, 1984;Siwicki et al, 1985;Marder et al, 1986;Siwicki and Bishop, 1986;Stangier et al, 1986;Beltz et al, 1990;Orchard, 1989 for review on insects). In motorneurons, it is thought to coexist with the excitatory transmitter glutamate (Witten and O'Shea, 1985;Bishop et al, 1987;Bartos et al, 1994).…”

Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila

“…These applications of exogenous biogenic amines likely mimic the roles of amines and͞or noradrenaline provided to the nerve or spinal cord from the brain by descending projections that are found in both vertebrates and insects (18,19). The invertebrate nerve cord differs from the higher vertebrate spinal cord in that the nerve cord contains aminergic cells bodies (20)(21)(22)(23). Presumably these cell bodies provide localized sources of amines to regions of the nerve cord neuropil that are not accessed by the descending aminergic projections.…”