Precraniate origin of cranial motoneurons

Abstract

The craniate head is innervated by cranial sensory and motor neurons. Cranial sensory neurons stem from the neurogenic placodes and neural crest and are seen as evolutionary innovations crucial in fulfilling the feeding and respiratory needs of the craniate ''new head.'' In contrast, cranial motoneurons that are located in the hindbrain and motorize the head have an unclear phylogenetic status. Here we show that these motoneurons are in fact homologous to the motoneurons of the sessile postmetamorphic form of ascidians. The motoneurons of adult Ciona intestinalis, located in the cerebral ganglion and innervating muscles associated with the huge ''branchial basket,'' express the transcription factors CiPhox2 and CiTbx20, whose vertebrate orthologues collectively define cranial motoneurons of the branchiovisceral class. Moreover, Ciona's postmetamorphic motoneurons arise from a hindbrain set aside during larval life and defined as such by its position (caudal to the prosensephalic sensory vesicle) and coexpression of CiPhox2 and CiHox1, whose orthologues collectively mark the vertebrate hindbrain. These data unveil that the postmetamorphic ascidian brain, assumed to be a derived feature, in fact corresponds to the vertebrate hindbrain and push back the evolutionary origin of cranial nerves to before the origin of craniates.Ciona intestinalis ͉ development ͉ evolution ͉ hindbrain

Early crest animals and the insight they provide into the evolutionary origin of craniates

“…The discovery of the Lower Cambrian tunicate Shankouclava , however, indicates that this animal group had already diverged morphologically from the main evolutionary course of the vertebrates by the Early Cambrian. Despite being departed from the main vertebrate evolutionary course for more than half a billion years and showing no crucial features in either its body plan (Lacalli, 2005) or genome (Holland, 2007) to link it directly to vertebrates in some aspects, tunicates yield many interesting clues that contribute to the dis- cussion of the evolutionary origin of the vertebrates with respect to neural crest cells (Jeffery et al, 2007), brain (Dufour et al, 2006), heart (Davidson and Levine, 2003;Simões-Costa et al, 2005), and eye lens (Shimeld and Purkiss, 2005).…”

A human mutation in Phox2b causes lack of CO 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons

“…For in situ hybridization and immunohistochemistry, brains were fixed in 4% paraformaldehyde and analyzed on sagittal or coronal cryosections of 12 m. Fluorescent in situ hybridization with vGlut2 and Phox2b riboprobes labeled with digoxygenin (DIG) and FITC, respectively, was done as described (47,48). Briefly, the sections were hybridized simultaneously with both probes, followed by sequential incubations with horseradish peroxidase-coupled anti-FITC Fab and FITC-tyramide working solution (PerkinElmer).…”

Molecular Interaction between Projection Neuron Precursors and Invading Interneurons via Stromal-Derived Factor 1 (CXCL12)/CXCR4 Signaling in the Cortical Subventricular Zone/Intermediate Zone

“…Dll-DLX polyclonal rabbit IgG (Panganiban et al, 1995) was used 1:100. To detect proliferating cell nuclear antigen (PCNA; MAB377, 1:100; Chemicon, Temecula, CA) and Cux1 , 1:100; Santa Cruz Biotechnology, Santa Cruz, CA), sections were pretreated in boiling 10 mM citric acid, pH 6, for 60 s. For double fluorescent ISH (FISH), sections were cohybridized with a digoxigenin (DIG)-labeled SDF probe and an FITClabeled Cux2 probe or with a DIG-labeled CXCR4 probe and an FITClabeled Lhx6 probe and processed as described by Dufour et al (2006).…”