Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: Ultrastructure and immunoreactivity to serotonin

Page, Louise R.; Parries, Shawn C

doi:10.1002/(sici)1096-9861(20000320)418:4<383::aid-cne2>3.0.co;2-b

Cited by 82 publications

(122 citation statements)

References 48 publications

Supporting

Mentioning

119

Contrasting

Order By: Relevance

“…No innervation of the prototroch by serotonergic nerves was observed. Kempf et al ('97), Page and Parries (2000), and Schaefer and Ruthensteiner (2001) described apical organs of some gastropods in fine detail. They found four main types of cells, ciliary tuft cells (apparently non-sensory), ampullary sensory neurons (with a group of cilia in a deep, narrow invagination), para-ampullary sensory neurons (with two short cilia at the surface of the epithelium), and non-sensory neurons.…”

Section: Apical Organ and Adult Brainsupporting

confidence: 94%

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

2004

View full text Add to dashboard Cite

The trochophora concept and the literature on cleavage patterns and differentiation of ectodermal structures in annelids (''polychaetes'') and molluscs are reviewed. The early development shows some variation within both phyla, and the cephalopods have a highly modified development. Nevertheless, there are conspicuous similarities between the early development of the two phyla, related to the highly conserved spiral cleavage pattern. Apical and cerebral ganglia have almost identical origin in the two phyla, and the cell-lineage of the prototroch is identical, except for minor variations between species. The cell-lineage of the metatrochs is almost unknown, but the telotroch of annelids and the ''telotroch'' of the gastropod Patella originate from the 2d-cell, as does the gastrotroch in the few species which have been studied. The segmented annelid body, i.e. the region behind the peristome, develops through addition of new ectoderm from a ring of 2d-cells just in front of the telotroch. This whole region is thus derived from 2d-cells. Conversely, the mollusc body is covered by descendants of cells from both the C and D quadrants and a growth zone is not apparent. This supports the notion that the molluscs are not segmented like the annelids, and that the repeated structures seen in polyplacophorans and monplacophorans do not represent a segmentation homologous to that of the annelids.

show abstract

Section: Apical Organ and Adult Brainsupporting

confidence: 94%

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

2004

View full text Add to dashboard Cite

show abstract

“…Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11)(12)(13)(14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17)(18)(19)(20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22)(23)(24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.…”

mentioning

confidence: 69%

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Conzelmann

Williams

Tunaru

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

216

View full text Add to dashboard Cite

Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory-neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii. MIP is expressed in chemosensory-neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor-ligand pair in regulating marine annelid settlement.M etazoan life cycles show great diversity in larval, juvenile, and adult forms, as well as in the timing and ecological context of the transitions between these forms. In many animal species, neuroendocrine signals involving hormones and neuropeptides regulate life cycle transitions (1-3). Environmental cues are often important instructors of the timing of life cycle transitions (4), and can affect behavioral, physiological, or morphological change via neuroendocrine signaling (5).Marine invertebrate larval settlement is a prime example of the strong link between environmental cues and the timing of life-cycle transitions. Marine invertebrate life cycles often consist of a free-swimming (i.e., pelagic) larval stage that settles to the ocean floor and metamorphoses into a bottom-dwelling (i.e., benthic) juvenile (6-8). In many invertebrate larvae, a pelagicbenthic transition is induced by chemical cues from the environment (9, 10). Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11-14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17-20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22-24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.Here, we identify a conserved myoinhibitory peptide (MIP)/ allatostatin-B receptor-ligand pair as a regulator of larval settlement behavior in the marine polychaete annelid Platynereis dumerilii. MIPs are pleiotro...

show abstract

“…1999; Kempf et al, 1997;Page and Parries, 2000) and bivalves (Croll et al, 1997;Plummer, 2002), although the cell types of the targets are generally unknown. Finally, physiological evidence also exists suggesting that momentary arrests of preoral cilia on the velum might be elicited by neural input (Arkett, 1987;Leise and Hadfield, 2000).…”

Section: Introductionmentioning

confidence: 99%

“…Although these findings may be generally applicable to closely related species (Uhler et al, 2000), questions arise about whether direct-developing pulmonate gastropods are representative models for understanding the control of ciliary activity on vela of freeliving molluscan larvae. In particular, ciliated cells on the foot of H. trivolvis are only known to possess serotonergic innervation whereas serotonergic, catecholaminergic and peptidergic axons extend into the vela of larval caenogastropods (Dickinson and Croll, 2003;Dickinson et al, 1999;Page and Parries, 2000), heterobranch gastropods (Dickinson et al, 2000;Kempf et al, 1997) and bivalves (Croll et al, 1997;Plummer, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…Subtle changes in the tone of this muscle could also reposition the velum and affect the direction of swimming. Neural innervation of the velar musculature has been described in developing caenogastropods (Dickinson and Croll, 2003;Page and Parries, 2000) and heterobranchs (Kempf et al, 1997), but it remains unclear how this innervation contributes to maintenance and control of muscle activity.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Braubach

Dickinson

Evans

et al. 2006

Journal of Experimental Biology

View full text Add to dashboard Cite

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.

show abstract

Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: Ultrastructure and immunoreactivity to serotonin

Cited by 82 publications

References 48 publications

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

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

Contact Info

Product

Resources

About