Abstract:Cephalopods are unique among mollusks in exhibiting an elaborate central nervous system (CNS) and remarkable cognitive abilities. Despite a profound knowledge of the neuroanatomy and neurotransmitter distribution in their adult CNS, little is known about the expression of neurotransmitters during cephalopod development. Here, we identify the first serotonin-immunoreactive (5-HT-ir) neurons during ontogeny and describe the establishment of the 5-HT system in the pygmy squid, Idiosepius notoides. Neurons that ar… Show more
“…Here we concentrate on the period of differentiation, from stages E24 through E27, although we comment briefly on SoxB1 and SoxE expression during the disc phase (stage E18: see below). Nomenclature of the developing nervous system follows that described in [ 54 , 55 ], [ 8 ], and [ 5 ]. For ease of comparison with other molluscan systems, we adopt the embryonic axes as described in [ 56 ] wherein the mouth and brachial arm crown corresponds to the ventral surface, and the funnel is located posteriorly.…”
Cephalopods provide an unprecedented opportunity for comparative studies of the developmental genetics of organ systems that are convergent with analogous vertebrate structures. The Sox-family of transcription factors is an important class of DNA-binding proteins that are known to be involved in many aspects of differentiation, but have been largely unstudied in lophotrochozoan systems. Using a degenerate primer strategy we have isolated coding sequence for three members of the Sox family of transcription factors from a cephalopod mollusk, the European cuttlefish Sepia officinalis: Sof-SoxE, Sof-SoxB1, and Sof-SoxB2. Analyses of their expression patterns during organogenesis reveals distinct spatial and temporal expression domains. Sof-SoxB1 shows early ectodermal expression throughout the developing epithelium, which is gradually restricted to presumptive sensory epithelia. Expression within the nervous system appears by mid-embryogenesis. Sof-SoxB2 expression is similar to Sof-SoxB1 within the developing epithelia in early embryogenesis, however appears in largely non-overlapping expression domains within the central nervous system and is not expressed in the maturing sensory epithelium. In contrast, Sof-SoxE is expressed throughout the presumptive mesodermal territories at the onset of organogenesis. As development proceeds, Sof-SoxE expression is elevated throughout the developing peripheral circulatory system. This expression disappears as the circulatory system matures, but expression is maintained within undifferentiated connective tissues throughout the animal, and appears within the nervous system near the end of embryogenesis. SoxB proteins are widely known for their role in neural specification in numerous phylogenetic lineages. Our data suggests that Sof-SoxB genes play similar roles in cephalopods. In contrast, Sof-SoxE appears to be involved in the early stages of vasculogenesis of the cephalopod closed circulatory system, a novel role for a member of this gene family.
“…Here we concentrate on the period of differentiation, from stages E24 through E27, although we comment briefly on SoxB1 and SoxE expression during the disc phase (stage E18: see below). Nomenclature of the developing nervous system follows that described in [ 54 , 55 ], [ 8 ], and [ 5 ]. For ease of comparison with other molluscan systems, we adopt the embryonic axes as described in [ 56 ] wherein the mouth and brachial arm crown corresponds to the ventral surface, and the funnel is located posteriorly.…”
Cephalopods provide an unprecedented opportunity for comparative studies of the developmental genetics of organ systems that are convergent with analogous vertebrate structures. The Sox-family of transcription factors is an important class of DNA-binding proteins that are known to be involved in many aspects of differentiation, but have been largely unstudied in lophotrochozoan systems. Using a degenerate primer strategy we have isolated coding sequence for three members of the Sox family of transcription factors from a cephalopod mollusk, the European cuttlefish Sepia officinalis: Sof-SoxE, Sof-SoxB1, and Sof-SoxB2. Analyses of their expression patterns during organogenesis reveals distinct spatial and temporal expression domains. Sof-SoxB1 shows early ectodermal expression throughout the developing epithelium, which is gradually restricted to presumptive sensory epithelia. Expression within the nervous system appears by mid-embryogenesis. Sof-SoxB2 expression is similar to Sof-SoxB1 within the developing epithelia in early embryogenesis, however appears in largely non-overlapping expression domains within the central nervous system and is not expressed in the maturing sensory epithelium. In contrast, Sof-SoxE is expressed throughout the presumptive mesodermal territories at the onset of organogenesis. As development proceeds, Sof-SoxE expression is elevated throughout the developing peripheral circulatory system. This expression disappears as the circulatory system matures, but expression is maintained within undifferentiated connective tissues throughout the animal, and appears within the nervous system near the end of embryogenesis. SoxB proteins are widely known for their role in neural specification in numerous phylogenetic lineages. Our data suggests that Sof-SoxB genes play similar roles in cephalopods. In contrast, Sof-SoxE appears to be involved in the early stages of vasculogenesis of the cephalopod closed circulatory system, a novel role for a member of this gene family.
“…These masses comprise various individual lobes (up to 35 in some coleoid cephalopods), which are subject to increased neuropilar growth and a relative decrease of perikarya during subsequent development. The adult CNS of I. notoides resembles that of its sister species I. paradoxus [ 8 , 12 , 13 , 49 ]. It is composed of a central brain and two laterally attached optic lobes that process the visual stimuli from the laterally attached eyes.…”
Section: Resultsmentioning
confidence: 99%
“…These studies revealed that selected neuropeptides and neurotransmitters are expressed during early CNS development and thus appear to play a role during early neurogenesis [ 11 – 16 ]. They also suggest that certain neuronal populations that contain these substances might be homologous among coleoids [ 12 , 13 , 16 ]. Figure 1 Sketch drawings highlighting the development of individual ganglia into a centralized brain in I. notoides .…”
BackgroundAmong the Lophotrochozoa, cephalopods possess the highest degree of central nervous system (CNS) centralization and complexity. Although the anatomy of the developing cephalopod CNS has been investigated, the developmental mechanisms underlying brain development and evolution are unknown. POU genes encode key transcription factors controlling nervous system development in a range of bilaterian species, including lophotrochozoans. In this study, we investigate the expression of POU genes during early development of the pygmy squid Idiosepius notoides and make comparisons with other bilaterians to reveal whether these genes have conserved or divergent roles during CNS development in this species.ResultsPOU2, POU3, POU4 and POU6 orthologs were identified in transcriptomes derived from developmental stages and adult brain tissue of I. notoides. All four POU gene orthologs are expressed in different spatiotemporal combinations in the early embryo. Ino-POU2 is expressed in the gills and the palliovisceral, pedal, and optic ganglia of stage 19 to 20 embryos, whereas the cerebral and palliovisceral ganglia express Ino-POU3. Ino-POU4 is expressed in the optic and palliovisceral ganglia and the arms/intrabrachial ganglia of stage 19 to 20 individuals. Ino-POU6 is expressed in the palliovisceral ganglia during early development. In stage 25 embryos expression domains include the intrabrachial ganglia (Ino-POU3) and the pedal ganglia (Ino-POU6). All four POU genes are strongly expressed in large areas of the brain of stage 24 to 26 individuals. Expression could not be detected in late prehatching embryos (approximately stage 27 to 30).ConclusionsThe expression of four POU genes in unique spatiotemporal combinations during early neurogenesis and sensory organ development of I. notoides suggests that they fulfill distinct tasks during early brain development. Comparisons with other bilaterian species reveal that POU gene expression is associated with anteriormost neural structures, even between animals for which these structures are unlikely to be homologous. Within lophotrochozoans, POU3 and POU4 are the only two genes that have been comparatively investigated. Their expression patterns are broadly similar, indicating that the increased complexity of the cephalopod brain is likely due to other unknown factors.
“…The whole-mount immunofluorescence method had been employed to investigate the development of nervous system in mollusc larvae [10,17,32,35,36]. In the present study, to further understand the development of catecholaminergic nervous system, the CfDDC and CfDBH immunoreactive cells were detected simultaneously by the whole-mount immunofluorescence method in scallop larvae.…”
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