Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain

Murakami, Yasunori; Pasqualetti, Massimo; Takio, Yoko; Hirano, Shigeki; Rijli, Filippo M.; Kuratani, Shigeru

doi:10.1242/dev.00986

Cited by 109 publications

(121 citation statements)

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“…The pTRG is intrinsically rhythmically active and glutamatergic, and projects to vagal motor neurons (Cinelli et al, 2013), features shared with the Xenopus DTAM vocal circuit (reviewed in Zornik and Kelley, 2017). Both the pTRG and DTAM are located in the rostral hindbrain compartment derived from embryonic rhombomere 1 (r1; Murakami et al, 2004;Morona and González, 2009). The several shared features described above support the homology of DTAM to the pTRG.…”

Section: Evolution Of Hindbrain Circuits What Is Dtam? Hindbrain Circmentioning

confidence: 99%

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

Barkan

Zornik

Kelley

2016

Journal of Experimental Biology

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The neural circuits underlying divergent courtship behaviors of closely related species provide a framework for insight into the evolution of motor patterns. In frogs, male advertisement calls serve as unique species identifiers and females prefer conspecific to heterospecific calls. Advertisement calls of three relatively recently (∼8.5 Mya) diverged species -Xenopus laevis, X. petersii and X. victorianusinclude rapid trains of sound pulses (fast trills). We show that while fast trills are similar in pulse rate (∼60 pulses s) across the three species, they differ in call duration and period (time from the onset of one call to the onset of the following call). Previous studies of call production in X. laevis used an isolated brain preparation in which the laryngeal nerve produces compound action potentials that correspond to the advertisement call pattern (fictive calling). Here, we show that serotonin evokes fictive calling in X. petersii and X. victorianus as it does in X. laevis. As in X. laevis, fictive fast trill in X. petersii and X. victorianus is accompanied by an N-methyl-D-aspartate receptordependent local field potential wave in a rostral hindbrain nucleus, DTAM. Across the three species, wave duration and period are strongly correlated with species-specific fast trill duration and period, respectively. When DTAM is isolated from the more rostral forebrain and midbrain and/or more caudal laryngeal motor nucleus, the wave persists at species-typical durations and periods. Thus, intrinsic differences within DTAM could be responsible for the evolutionary divergence of call patterns across these related species.

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Section: Evolution Of Hindbrain Circuits What Is Dtam? Hindbrain Circmentioning

confidence: 99%

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

Barkan

Zornik

Kelley

2016

Journal of Experimental Biology

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“…Within the HB, which in vertebrates is both morphologically and molecularly subdivided into rhombomeres (Lumsden and Krumlauf, 1996), AP patterning is generally controlled by a hox code involving nested collinear expression of hox genes along the AP axis, which defines the identity of each rhombomere (Trainor and Krumlauf, 2001). It is well established that RA regulates this collinear expression of hox genes in the vertebrate HB (Glover et al, 2006;Murakami et al, 2004). Treatments with RA induce an anterior expansion of the HB and the spinal cord (SC) and inhibit formation of anterior brain structures, such as the forebrain (FB) and the midbrain (MB) (Durston et al, 1989).…”

Section: Patterning Of the Central Nervous System And Neuronal Differmentioning

confidence: 99%

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Campo-Paysaa

Marlétaz

Laudet

et al. 2008

Genesis

118

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Summary: Retinoic acid (RA) is a vitamin A-derived morphogen important for axial patterning and organ formation in developing vertebrates and invertebrate chordates (tunicates and cephalochordates). Recent analyses of genomic data have revealed that the molecular components of the RA signaling cascade are also present in other invertebrate groups, such as hemichordates and sea urchins. In this review, we reassess the evolutionary origins of the RA signaling pathway by examining the presence of key factors of this signaling cascade in different metazoan genomes and by comparing tissue-specific roles for RA during development of different animals. This discussion of genomic and developmental data suggests that RA signaling might have originated earlier in metazoan evolution than previously thought. On the basis of this hypothesis, we conclude by proposing a scenario for the evolution of RA functions during development, which highlights functional gains and lineage-specific losses during metazoan diversification. genesis 46:640-656,

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“…This concurs with the fact that targeted mutation of Hoxa2 in mice leads to partial duplication of the lower jaw at the expense of the normal BA2 skeleton (the hyoid cartilage) (Gendron-Maguire et al, 1993;Rijli et al, 1993;Kanzler et al, 1998;Ohnemus et al, 2001). In the lamprey (Lampetra fluviatilis), a jawless vertebrate, the forepole of the embryo does not express Hox3 (Murakami et al, 2004), whereas, as observed by Cohn (Cohn, 2002), the HoxL6 gene (the lamprey homologue of vertebrate Hoxb6) does not obey the colinearity rule (between Hox gene organisation in the chromosome and the anterior limit of their expression in the embryo). The HoxL6 expression domain reaches the rostral-most part of the embryo.…”

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confidence: 95%

“…In the lamprey (Lampetra fluviatilis), a jawless vertebrate, the forepole of the embryo does not express Hox3 (Murakami et al, 2004), whereas, as observed by Cohn (Cohn, 2002), the HoxL6 gene (the lamprey homologue of vertebrate Hoxb6) does not obey the colinearity rule (between Hox gene organisation in the chromosome and the anterior limit of their expression in the embryo). The HoxL6 expression domain reaches the rostral-most part of the embryo.…”

mentioning

confidence: 95%

Neural crest cell plasticity and its limits

et al. 2004

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The quail-chick chimera system (see Box 1) has been used over the years to establish a fate map of the NC along the neural axis. These studies have shown that melanocytes arise from the entire length of the NC in higher vertebrates, whereas mesectodermal derivatives originate only from the cephalic NC region. NC-derived cells that contribute to the PNS and ENS arise only from some areas of the neural axis (Fig. 1).Using the quail-chick system, well-defined areas of the NC have been exchanged to assess NCC plasticity (see Fig. 1). For example, in one study, the vagal region of the NC (which is located between somites 1 and 7, and gives rise to the enteric ganglia) was exchanged with NC from between somites 18 and 24 (which gives rise to the adrenal medulla and sympathetic ganglia) (Le Douarin and Teillet, 1974). This swap resulted Review 4638 in the normal colonisation of the suprarenal gland and sympathetic ganglia by NCCs fated to colonise the gut. However, although the adrenomedullary trunk NCCs invaded the pre-umbilical gut wall and differentiated into normal enteric plexuses, they failed to reach the post-umbilical bowel .This experimental system has since been used together with various molecular markers, such as the Schwann cell myelin protein (SMP), which is present on Schwann cells but not on other PNS and ENS glial cells, to allow a more refined analysis of NCC plasticity. These studies have shown that NCC differentiation into a specific type of glia depends upon the environment in which they develop (Dulac et al., 1988;Dulac and Le Douarin, 1991; Cameron-Curry et al., 1993). Similarly, the differentiation of the various types of autonomic neurons varies according to the milieu in which they differentiate (for reviews, see Le Douarin, 1982;Le Douarin and Kalcheim, 1999).The conclusion of these heterotopic grafting experiments was that the fate of the NCCs that form the PNS and ENS is not fully determined before these cells migrate, but instead remains plastic until they receive differentiation signals at the end of, and possibly during, their migration. This finding raised the issue of whether all the precursors of PNS ganglion cells became fully differentiated and/or committed soon after reaching their sites of arrest, or whether some remained as quiescent undifferentiated cells. This was explored in the experiments discussed in the following section. Undifferentiated precursors in PNS gangliaTo investigate the developmental potentials of PNS ganglion cells, fragments of sensory and autonomic ganglia from quail embryos, taken from embryonic day (E) 4 up to the end of the incubation period, were implanted into NCC migration pathways of E2 chick hosts when their own NCCs were migrating. The grafted neurons themselves died (probably because the necessary survival factors are not present in the younger host). However, the non-neuronal cells of implanted ganglia migrated and homed to host sensory and autonomic ganglia, where they differentiated into the types of neurons and glia corresponding to their novel...

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Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain

Cited by 109 publications

References 103 publications

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

Evolution of vocal patterns: tuning hindbrain circuits during species divergence

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

Neural crest cell plasticity and its limits

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