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Open Access Highly Accessed Research article

Ancient origin of somatic and visceral neurons

Marc Nomaksteinsky12, Stefan Kassabov3, Zoubida Chettouh12, Henri-Corto Stoeklé12, Laure Bonnaud4, Gilles Fortin5, Eric R Kandel367 and Jean-François Brunet12*

Author affiliations

1 Institut de Biologie de l’École normale supérieure (IBENS), CNRS UMR8197, INSERM U1024, Paris, France

2 Paris Sciences et Lettres University, Paris, France

3 Department of Neuroscience, College of Physicians and Surgeons of Columbia University, New York, USA

4 Museum National d’Histoire Naturelle, CNRS UMR7208, Université Pierre et Marie Curie, Paris, France

5 Institut de Neurobiologie Alfred Fessard, CNRS UPR3294, Gif-sur-Yvette, 91198, France

6 Howard Hughes Medical Institute, College of Physicians and Surgeons of Columbia University, New York, USA

7 Kavli Institute for Brain Science, College of Physicians and Surgeons of Columbia University, New York, USA

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Citation and License

BMC Biology 2013, 11:53  doi:10.1186/1741-7007-11-53

Published: 30 April 2013

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+/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.

Results

We 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.

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.

Keywords:
Sensory neurons; Motor neurons; Evolution; Transcription factors; Mollusks; Lophotrochozoa; Lymnaea; Aplysia; Sepia; Phox2; Brn3; Mnx