Ancient origin of somatic and visceral neurons. - Archive ouverte HAL Access content directly
Journal Articles BMC Biology Year : 2013

Ancient origin of somatic and visceral neurons.

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Abstract

BACKGROUND: A key to understanding the evolution of the nervous system on a large phylogenetic scale is the identification of homologous neuronal types. Here, we focus this search on the sensory and motor neurons of bilaterians, exploiting their well-defined molecular signatures in vertebrates. Sensorimotor circuits in vertebrates are of two types: somatic (that sense the environment and respond by shaping bodily motions) and visceral (that sense the interior milieu and respond by regulating vital functions). These circuits differ by a small set of largely dedicated transcriptional determinants: Brn3 is expressed in many somatic sensory neurons, first and second order (among which mechanoreceptors are uniquely marked by the Brn3+/Islet+/Drgx+ signature), somatic motoneurons uniquely co-express Lhx3/4 and Mnx1, while the vast majority of neurons, sensory and motor, involved in respiration, blood circulation or digestion are molecularly defined by their expression and dependence on the pan-visceral determinant Phox2b. RESULTS: We explore the status of the sensorimotor transcriptional code of vertebrates in mollusks, a lophotrochozoan clade that provides a rich repertoire of physiologically identified neurons. In the gastropods Lymnaea stagnalis and Aplysia californica, we show that homologues of Brn3, Drgx, Islet, Mnx1, Lhx3/4 and Phox2 differentially mark neurons with mechanoreceptive, locomotory and cardiorespiratory functions. Moreover, in the cephalopod Sepia officinalis, we show that Phox2 marks the stellate ganglion (in line with the respiratory --- i.e. visceral--- ancestral role of the mantle, its target organ), while the anterior pedal ganglion, which controls the prehensile and locomotory arms, expresses Mnx. CONCLUSIONS: Despite considerable divergence in overall neural architecture, a molecular underpinning for the functional allocation of neurons to interactions with the environment or to homeostasis was inherited from the urbilaterian ancestor by contemporary protostomes and deuterostomes.
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Dates and versions

inserm-00824421 , version 1 (21-05-2013)

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Marc Nomaksteinsky, Stefan Kassabov, Zoubida Chettouh, Henri-Corto Stoeklé, Laure Bonnaud, et al.. Ancient origin of somatic and visceral neurons.. BMC Biology, 2013, 11 (1), pp.53. ⟨10.1186/1741-7007-11-53⟩. ⟨inserm-00824421⟩
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