Ancient origin of somatic and visceral neurons View Full Text


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Article Info

DATE

2013-04-30

AUTHORS

Marc Nomaksteinsky, Stefan Kassabov, Zoubida Chettouh, Henri-Corto Stoeklé, Laure Bonnaud, Gilles Fortin, Eric R Kandel, Jean-François Brunet

ABSTRACT

BackgroundA 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+/Islet1+/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.ResultsWe explore the status of the sensorimotor transcriptional code of vertebrates in mollusks, a lophotrochozoa 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, Islet1, Mnx1, Lhx3/4 and Phox2b 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 — that is, visceral— ancestral role of the mantle, its target organ), while the anterior pedal ganglion, which controls the prehensile and locomotory arms, expresses Mnx.ConclusionsDespite 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. More... »

PAGES

53

References to SciGraph publications

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    URI

    http://scigraph.springernature.com/pub.10.1186/1741-7007-11-53

    DOI

    http://dx.doi.org/10.1186/1741-7007-11-53

    DIMENSIONS

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    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/23631531


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    31 schema:description BackgroundA 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+/Islet1+/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.ResultsWe explore the status of the sensorimotor transcriptional code of vertebrates in mollusks, a lophotrochozoa 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, Islet1, Mnx1, Lhx3/4 and Phox2b 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 — that is, visceral— ancestral role of the mantle, its target organ), while the anterior pedal ganglion, which controls the prehensile and locomotory arms, expresses Mnx.ConclusionsDespite 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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    37 schema:keywords Aplysia californica
    38 Brn3
    39 Islet1
    40 Lophotrochozoa clade
    41 Lymnaea stagnalis
    42 MNX
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    44 Phox2
    45 Phox2b
    46 ResultsWe
    47 Sepia officinalis
    48 allocation
    49 ancestor
    50 ancient origin
    51 architecture
    52 arm
    53 bilaterians
    54 blood circulation
    55 californica
    56 cardiorespiratory function
    57 cephalopod Sepia officinalis
    58 circuit
    59 circulation
    60 clade
    61 code
    62 considerable divergence
    63 dependence
    64 determinants
    65 deuterostomes
    66 digestion
    67 divergence
    68 environment
    69 evolution
    70 expression
    71 function
    72 functional allocation
    73 ganglia
    74 gastropod Lymnaea stagnalis
    75 homologues
    76 identification
    77 interaction
    78 key
    79 large phylogenetic scale
    80 locomotory
    81 majority
    82 molecular signatures
    83 molecular underpinnings
    84 mollusks
    85 motoneurons
    86 motor
    87 motor neurons
    88 nervous system
    89 neural architecture
    90 neuronal types
    91 neurons
    92 officinalis
    93 order
    94 origin
    95 pedal ganglia
    96 phylogenetic scale
    97 prehensile
    98 protostomes
    99 repertoire
    100 respiration
    101 rich repertoire
    102 scale
    103 search
    104 second order
    105 sensorimotor circuits
    106 sensory
    107 sensory neurons
    108 set
    109 signatures
    110 small set
    111 somatic motoneurons
    112 somatic sensory neurons
    113 stagnalis
    114 status
    115 stellate ganglion
    116 system
    117 transcriptional code
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