Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails

Croll, Roger P.

doi:10.1002/1097-0029(20000615)49:6<570::aid-jemt7>3.0.co;2-q

Cited by 43 publications

(40 citation statements)

References 57 publications

(63 reference statements)

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“…Developmental studies attribute primarily tropic and trophic actions to certain peptides, including induction of neurogenesis and effects on neuronal migration (Strand et al, 1991;De Felipe et al, 1995;Voronezhskaya and Elekes, 1996;Croll, 2000;Hökfelt et al, 2000;Yacubova and Komuro, 2002). A few studies suggest important functions of peptides especially in the developing or regenerating olfactory system.…”

Section: Possible Roles Of Mas-at and Other Neuropeptides During Al Dmentioning

confidence: 99%

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

Utz

Huetteroth

Vömel

et al. 2007

Developmental Neurobiology

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ABSTRACT:The paired antennal lobes (ALs) of the sphinx moth Manduca sexta serve as a well-established model for studying development of the primary integration centers for odor information in the brain. To further reveal the role of neuropeptides during AL development, we have analyzed cellular distribution, developmental time course, and regulation of the neuropeptide M. sexta allatotropin (Mas-AT). On the basis of morphology and appearance during AL formation, seven major types of Mas-AT-immunoreactive (ir) cells could be distinguished. Mas-AT-ir cells are identified as local, projection, and centrifugal neurons, which are either persisting larval or newly added adult-specific neurons. Complementary immunostaining with antisera against two other neuropeptide families (A-type allatostatins, RFamides) revealed colocalization within three of the Mas-AT-ir cell types. On the basis of this neurochemistry, the most prominent type of Mas-AT-ir neurons, the local AT neurons (LATn), could be divided in three subpopulations. The appearance of the Mas-AT-ir cell types occurring during metamorphosis parallels the rising titer of the developmental hormone 20-hydroxyecdysone (20E). Artificially shifting the 20E titer to an earlier developmental time point resulted in the precocious occurrence of Mas-AT immunostaining. This result supports the hypothesis that the pupal rise of 20E is causative for Mas-AT expression during AL development. Comparing localization and developmental time course of Mas-AT and other neuropeptides with the time course of AL formation suggests various functions for these neuropeptides during development, including an involvement in the formation of the olfactory glomeruli. '

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Section: Possible Roles Of Mas-at and Other Neuropeptides During Al Dmentioning

confidence: 99%

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

Utz

Huetteroth

Vömel

et al. 2007

Developmental Neurobiology

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“…These neuropeptides are thought to play a role in activity dependent tuning of intrinsic and synaptic properties of the developing stomatogastric ganglion pattern generator . In molluscs, neurons labeled with an FMRFamide antiserum occur very early in embryonic development and it is speculated that they might be involved in neurogenesis (Voronezhskaya and Elekes, 1996;Croll, 2000). Recent data from the developing or regenerating mouse olfactory epithelium demonstrated a role of two neuropeptides (neuropeptide Y and pituitary adenylate cyclase-activating polypeptide) in initiating proliferation of basal cells (Hansel et al, 2001a,b).…”

Section: Possible Roles Of Farps During Nervous System Developmentmentioning

confidence: 99%

Development and steroid regulation of RFamide immunoreactivity in antennal-lobe neurons of the sphinx mothManduca sexta

Schachtner

Trosowski

D'Hanis

et al. 2004

Journal of Experimental Biology

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SUMMARY During metamorphosis, the insect nervous system undergoes considerable remodeling: new neurons are integrated while larval neurons are remodeled or eliminated. To understand further the mechanisms involved in transforming larval to adult tissue we have mapped the metamorphic changes in a particularly well established brain area, the antennal lobe of the sphinx moth Manduca sexta, using an antiserum recognizing RFamide-related neuropeptides. Five types of RFamide-immunoreactive (ir) neurons could be distinguished in the antennal lobe, based on morphology and developmental appearance. Four cell types (types II–V, each consisting of one or two cells) showed RFamide immunostaining in the larva that persisted into metamorphosis. By contrast, the most prominent group (type I), a mixed population of local and projection neurons consisting of about 60 neurons in the adult antennal lobe, acquired immunostaining in a two-step process during metamorphosis. In a first step, from 5 to 7 days after pupal ecdysis, the number of labeled neurons reached about 25. In a second step, starting about 4 days later, the number of RFamide-ir neurons increased within 6 days to about 60. This two-step process parallels the rise and fall of the developmental hormone 20-hydroxyecdysone (20E) in the hemolymph. Artificially shifting the 20E peak to an earlier developmental time point resulted in the precocious appearance of RFamide immunostaining and led to premature formation of glomeruli. Prolonging high 20E concentrations to stages when the hormone titer starts to decline had no effect on the second increase of immunostained cell numbers. These results support the idea that the rise in 20E, which occurs after pupal ecdysis, plays a role in the first phase of RFamide expression and in glomeruli formation in the developing antennal lobes. The role of 20E in the second phase of RFamide expression is less clear, but increased cell numbers showing RFamide-ir do not appear to be a consequence of the declining levels in 20E that occur during adult development.

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“…Serotonergic control of ciliary beating in developing molluscs has been best studied in the fresh water gastropod Helisoma trivolvis, which, like other pulmonates, develops in ovo and has a greatly reduced velum and larval nervous system (Croll, 2000;Croll and Dickinson, 2004). H. trivolvis uses a ciliated foot to rotate within the egg capsule to enhance aeration of the capsular fluid (Diefenbach et al, 1991;Marois and Croll, 1991).…”

Section: Introductionmentioning

confidence: 99%

Neural control of the velum in larvae of the gastropod,Ilyanassa obsoleta

Braubach

Dickinson

Evans

et al. 2006

Journal of Experimental Biology

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SUMMARY Larval molluscs commonly use ciliated vela to swim and feed. In this study we used immunohistochemistry to demonstrate innervation of velar cilia and muscles by monoaminergic and peptidergic fibres in the caenogastropod, Ilyanassa obsoleta. Photoelectric recordings from pre-oral cilia on isolated pieces of velum revealed that serotonin increased, whereas catecholamines (dopamine and norepinephrine) decreased beat frequency at concentrations of 10-6 to 10-9 mol l-1. Catecholamines also increased the frequency of momentary, isolated arrests of pre-oral cilia, but failed to suppress beating of the post-oral cilia at these concentrations. The neuropeptides, FMRFamide and Leu-enkephalin, did not affect the frequency of ciliary beating or of isolated ciliary arrests, but did induce numerous muscular contractions, which were accompanied by sustained ciliary arrests. In terms of whole animal behaviour, serotonin caused larvae to concentrate toward the top of a water column and to increase feeding,whereas catecholamines caused larvae to concentrate toward the bottom of a water column and decrease feeding. Monoamine analogues which facilitated or opposed the effects of synthetic transmitters on larval behaviour, further suggested that these transmitters are released endogenously to control velar function. Finally, applications of peptides to whole larvae caused increased frequency of locomotory arrests. Together these findings demonstrate several potential roles for the nervous system in controlling larval behaviour in gastropods.

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Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails

Cited by 43 publications

References 57 publications

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

Mas‐allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

Development and steroid regulation of RFamide immunoreactivity in antennal-lobe neurons of the sphinx mothManduca sexta

Neural control of the velum in larvae of the gastropod,Ilyanassa obsoleta

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