Ancient origin of somatic and visceral neurons

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.

Islet is a key determinant of ascidian palp morphogenesis

“…Islet is expressed in a wide variety of neurons across metazoans (Jackman et al, 2000;Nomaksteinsky et al, 2013;Simmons et al, 2012;Voutev et al, 2009). Though widely known for its role in motor neuron specification, it also functions in motor axon outgrowth in both Drosophila and vertebrates (Liang et al, 2011;Segawa et al, 2001;Thaler et al, 2004;Thor and Thomas, 1997).…”

Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

“…Phox2 binding to the CREST1 enhancer of Isl1 , which encodes the pan-motor neuronal transcription factor Islet1, is necessary for Islet1 expression in brainstem BMs and PVMs, and the Phox2 binding motif in CREST1 is highly conserved from lampreys to mammals (Kim, et al, 2015a). Phox2 expression specifically related to visceral neurons is already present in protostomes [represented by molluscs, (Nomaksteinsky, et al, 2013)]. In another major clade of deuterostomes, the echinoderms (represented by sea urchins) it is expressed in the developing CNS together with Nkx2.1 (Wygoda, et al, 2014), although it is unclear if this expression presages the differentiation of any specific type of motor neuron.…”

“…This strongly suggests that BMs and the transcription factors driving their specification evolved in the prechordate bilaterian lineage, and already in cephalochordates and urochordates were utilized specifically to innervate branchial musculature (Dufour, Chettouh, Deyts, De Rosa, Goridis, Joly and Brunet, 2006, Fritzsch and Northcutt, 1993a). It therefore appears likely that the branchial motor system formed at the base of the deuterostomes, possibly through modification of gene regulatory networks shared with protostome motor neuron development (Nomaksteinsky, Kassabov, Chettouh, Stoeklé, Bonnaud, Fortin, Kandel and Brunet, 2013). …”

Testing the evolutionary conservation of vocal motoneurons in vertebrates

“…The distinction between branchial and somatic motoneuron identity is proposed to be highly evolutionarily conserved (Butler and Hodos, 2005; Nomaksteinsky et al, 2013). Branchial, still often referred to as “special visceral”, motoneurons share a functional phenotype with motoneurons traditionally referred to as general somatic efferents that innervate muscle derived from somites, namely that both groups innervate skeletal, i.e.…”

“…For example, expression of the highly conserved Paired-like Homeobox 2 (Phox2) transcription factor (TF) gene family in branchial motoneurons in vertebrates and ingestion-related motoneurons in invertebrates has been used to argue for homology of these motorneuron populations (Dufour et al, 2006; Nomaksteinsky et al, 2013; Wilson et al, 2009). In mammals, laryngeal motoneurons express Phox2b during development, which persists in some neurons into adulthood.…”