Neurogenesis of cephalic sensory organs of Aplysia californica

Abstract

The opisthobranch gastropod Aplysia californica serves as a model organism in experimental neurobiology because of its simple and well-known nervous system. However, its nervous periphery has been less intensely studied. We have reconstructed the ontogeny of the cephalic sensory organs (labial tentacles, rhinophores, and lip) of planktonic, metamorphic, and juvenile developmental stages. FMRFamide and serotonergic expression patterns have been examined by immunocytochemistry in conjunction with epifluorescence and confocal laser scanning microscopy. We have also applied scanning electron microscopy to analyze the ciliary distribution of these sensory epithelia. Labial tentacles and the lip develop during metamorphosis, whereas rhinophores appear significantly later, in stage 10 juveniles. Our study has revealed immunoreactivity against FMRFamides and serotonin in all major nerves. The common labial nerve develops first, followed by the labial tentacle base nerve, oral nerve, and rhinophoral nerve. We have also identified previously undescribed neuronal pathways and other FMRFamide-like-immunoreactive neuronal elements, such as peripheral ganglia and glomerulus-like structures, and two groups of conspicuous transient FMRFamide-like cell somata. We have further found two distinct populations of FMRFamide-positive cell somata located both subepidermally and in the inner regions of the cephalic sensory organs in juveniles. The latter population partly consists of sensory cells, suggesting an involvement of FMRFamide-like peptides in the modulation of peripheral sensory processes. This study is the first concerning the neurogenesis of cephalic sensory organs in A. californica and may serve as a basis for future studies of neuronal elements in gastropod molluscs.

Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis

“…Glutamate-containing PSCs have been reported in sectioned CSOs of L. stagnalis (Hatakeyama et al, 2007), yet we have been unable to replicate this observation in either peripheral or CNS whole-mounts (unpublished observations). FMRFamide-immunoreactive PSCs have been described in a number of gastropod CSOs (Suzuki et al, 1997;Wollesen et al, 2007;Faller et al, 2008), but we were unable to achieve consistent labeling with antiFMRFamide (unpublished observations), and thus cannot confirm whether any are also present in L. stagnalis. PSCs in the CSOs of L. stagnalis have also been classified by using electron microscopy (Zylstra, 1972;Zaitseva and Bocharova, 1981;Roubos and van der Wal-Divendal, 1982), but the majority of cell types have morphologies that do not match any PSCs described here.…”

“…Histochemistry or immunohistochemistry have been used to describe putative catecholaminergic PSCs (Osborne and Cottrell, 1971;Salimova et al, 1987;Croll et al, 1999;Voronezhskaya et al, 1999;Croll, 2001;Croll et al, 2003), histaminergic PSCs (Hegedüs et al, 2004), nitregic PSCs (Elphick et al, 1995;Serfozo et al, 1998), FMRFamidergic PSCs (Nezlin et al, 1994a,b;Suzuki et al, 1997;Wollesen et al, 2007;Faller et al, 2008), and glutamatergic PSCs (Hatakeyama et al, 2007). In addition, putative chemosensory cells have been identified by using receptor signal transduction proteins (Mazzatenta et al, 2004;Cummins et al, 2009).…”

Mollusca

“…The velum is usually heavily innervated by serotonin-and FMRFa-LIR neurites that emerge from the apical organ and/or the cerebral commissure and disappear at metamorphosis (Dickinson et al 1999 ;Dickinson and Croll 2003 ;Wollesen et al 2007 ; see Croll 2009 for review). An additional pretrochal sense organ comprising two pairs of dorsolateral and two pairs of ventrolateral ampullary cells with a ciliated lumen that stain positive for FMRFamide and, less so, for serotonin has been found in polyplacophoran trochophores.…”

Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda)

“…The distribution of neurotransmitters in the CSOs of opisthobranchs has been studied in diVerent opisthobranch taxa (Salimova et al 1987;Moroz et al 1997;Croll 2001;Croll et al 2003;Wertz et al 2006Wertz et al , 2007Hochberg 2007;Wollesen et al 2007). These studies primarily focussed on the distribution of serotonin, whereas investigations of other neurotransmitters or neuropeptides were less extensive.…”