Precraniate origin of cranial motoneurons - PubMed (original) (raw)

Precraniate origin of cranial motoneurons

Héloïse D Dufour et al. Proc Natl Acad Sci U S A. 2006.

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.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.

Fig. 1.

Expression of CiPhox2 in embryos of C. intestinalis. Shown are lateral views (anterior to the right) of mid-tailbud-stage embryos (A and C_–_H) and a dorsal view of a late-tailbud-stage embryo (B) hybridized with the indicated probes. In the insets are shown higher magnifications of the _CiPhox2_-positive region. (A–F) CiPhox2 is coexpressed in a few cells behind the anlage of the sensory vesicle (A_–_C), together with CiPax2/5/8 (D), and partially overlapping caudally with CiHox1 (E and F). A Inset and B Inset feature magnifications illustrating the presence of four and eight CiPhox2-positive cells, respectively (asterisks). (C) Note that CiOtx is detected in axons projecting caudally from the sensory vesicle (arrowhead). (G and H) CiMnx is expressed in two domains, one caudal in unidentified cells and one rostral, marking part of the future visceral ganglion, where it is coexpressed with CiChAT (data not shown) in, presumably, the tail motoneurons. (H) Note the gap between CiMnx and CiPhox2, which may correspond to presumptive larval interneurons.

Fig. 2.

Fig. 2.

Expression of a CiPhox2::YFP transgene in the larva and during metamorphosis. (A Left_–_F Left) YFP-positive cells are detected in the larval neck (A Left) and at an equivalent position in neuronal precursors throughout metamorphosis, from early rotational (23) (B Left) to late rotational (23) (C Left and D), and juvenile (E and F) stages. (A Right_–_C Right) Schematic of larva and rotational stages of metamorphosis. (A Inset_–_C Inset and D Right_–_F Right) Magnifications of CiPhox2-positive cells. The type of long axon navigating around gill slits seen in D is no longer seen at juvenile stages, likely obscured by the thickness of the animal body wall. Fluorescence other than in neuronal precursors was either due to autofluorescence of apoptotic cells [e.g., in the degenerating tail (B_–_D) and CNS (D)] or spurious YFP expression (such as in the tunic in C and D). Neuronal expression was found in 80–90% of electroporated animals at all stages examined (51 larvae, 29 rotational stage animals, 8 juveniles, and 5 adults). ap, atriopore; e, endostyle; oo, otolith and ocellus; os, oral siphon; rt, tail in the process of resorption; s, stigmata; st, stomach.

Fig. 3.

Fig. 3.

Expression of the CiPhox2::YFP transgene in the cerebral ganglion of adult Ciona. (A) Diagram of the upper half of the adult Ciona showing the body wall muscle bands, the cerebral ganglion and major nerves (adapted from ref. 11). Note that some variability has been described in the arrangement of both nerves and muscle bands (11). ant.s.n., anterior siphonal nerves; g., cerebral ganglion; p., pericoronal nerve; post.s.n., posterior siphonal nerves; t.n., trunk nerves. (B) (Left) Dorsal view of the cerebral ganglion and its five canonical roots, plus an additional root rostrally on the left, all labeled with YFP. (Right) Schematic of the ganglion and roots. al, anterior left nerve ar, anterior right nerve; ln, lateral nerve (inconstant); pl, posterior left nerve; pr, posterior right nerve; vn, visceral nerve. (C) Lateral view of a transgenic adult animal showing the YFP-labeled cerebral ganglion, longitudinal nerves coursing along body wall muscle bands (superimposed on the right), and the pericoronal nerve (p) running across the oral siphon. (D_–_G) Magnifications of sections through the cortex of the ganglion hybridized with CiPhox2 (D), stained with DAPI (E), immunostained with an anti-CiPhox2 antibody (F), and hybridized with CiChAT (G).

Fig. 4.

Fig. 4.

Expression of Tbx20 in the CNS of mouse and Ciona. (A_–_D) Sections through the hindbrain of an embryonic-day-16.5 mouse embryo hybridized with a Tbx20 probe showing expression restricted to branchial and visceral motor nuclei: the trigeminal nucleus (nV) (A), the facial nucleus (nVII) (B), the nucleus ambiguus (nA) (C), the dorsal motor nucleus of the vagus nerve (dmnX) (D), and the accessory nucleus (nXI) (E), to the exclusion of somatic ones such as the hypoglossal (nXII in D) and abducens (data not shown). (F) (Left) Section through Ciona's cerebral ganglion hybridized with CiTbx20. (Right) Magnification of boxed area. The sense probe gave no signal (data not shown). (Scale bar, 100 μm.)

Fig. 5.

Fig. 5.

Homologies between rostrocaudal regions of the ascidian and vertebrate CNS and between their motoneuronal derivatives. (A) Previously proposed version of the ascidian tripartite brain model (4), based on gene expression in Halocynthia rorertzii. (B Upper) Rostrocaudal partition of the vertebrate CNS. (C Upper) Revised version of the ascidian larval brain model based on the present study. Regions of the CNS are color-coded as indicated in the key, according to the vertebrate nomenclature. Boxes on the left side of each model, color-coded as indicated in the key, demarcate neuroepithelial gene expression patterns used to define these regions. In mouse, Hox1 expression initially extends from rhombomere 4 to the caudal end of the spinal cord (41, 42) and is secondarily extinguished in the caudal myelencephalon (stippled light-gray box). In the previous version of the tripartite model (A), Phox2 was not examined and no overlap was detected between Pax2/5/8 and Hox1 (2). In the new model (C), both the pattern of Phox2 expression and its overlap with Hox1 lead to redefine the middle part of the larval brain as a hindbrain and to subdivide it into a posterior myelencephalon (blue) and an anterior metencephalon and/or MHB (pink and blue hatching). The trunk ganglion is homologous to the spinal cord, whereas the correspondence of the larval caudal cord (shaded in gray) with parts of the vertebrate CNS, if any, is uncertain. (B Lower and C Lower) Schematic of vertebrate (B Lower) and adult ascidian (C Lower) motoneurons color-coded according to, simultaneously, their origin and nature. Blue indicates branchiovisceral motoneurons born in the hindbrain; green indicates somatic motoneurons born in the spinal cord. No somatic motoneuron is detected in the ganglion of adult Ciona. In vertebrates, all branchiovisceral motor nuclei are born in the hindbrain, and somatic ones are born in the spinal cord except for the abducens (VI) and hypoglossal (XII), which were omitted for clarity.

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