Development of Neurogenic Placodes in Vertebrates

Abstract

The cranial sensory nervous system comprises a diverse set of organs: the eye, ear and nose and the sensory ganglia that transmit touch, pain, temperature and gustatory information to the brain. Despite the structural and functional diversity of the adult organs, during development, they arise from a common pool of sensory progenitor cells. These progenitors are specified early during embryonic development in the nonneural ectoderm next to the future brain. Subsequently, they diversify to form sensory placodes, special patches of thickened epithelium adjacent to the developing neural tube. Each placode acquires its unique identity under the influence of signals from surrounding tissues and later generates specialised cell types that characterise each organ.

Key Concepts

  • Evolution of elaborate sensory systems in the head allowed vertebrate evolution.
  • Sensory placodes are transient structures that form in the head ectoderm outside of the central nervous system and contribute to the sense organs and cranial sensory ganglia.
  • All sensory placodes arise from a pool of multipotent progenitors that have initially the potential to give rise to all placode derivatives, but their potential becomes restricted as the embryo develops. Placode progenitors develop in close association with central nervous system precursors and neural crest cells in a territory termed the ‘neural plate border’.
  • Placode progenitors are induced gradually in the ectoderm surrounding the anterior neural plate by signals from the underlying mesoderm. These signals differ along the rostro‐caudal axis with FGFs, BMP and Wnt antagonists inducing posterior progenitors, while anterior progenitors also require Shh and neuropeptides.
  • Localised sources of different signals induce olfactory, trigeminal, otic and epibranchial placodes from sensory progenitor cells.
  • Signals induce the expression of transcription factors in broad ectodermal domains, and mutual repression between them sharpen boundaries between neural, neural crest and placodal and between precursors for different placodes.

Keywords: BMP signalling; cell fate; ear; eye; FGF signalling; olfactory epithelium; transcription factors; Wnt signalling

Figure 1. Sensory placodes and their derivatives. (a) Diagram of a chick embryo at the 0‐somite stage. All sensory placodes arise from sensory progenitor cells (SPCs) located in the pre‐placodal region surrounding the neural plate (NP; grey). The pre‐placodal region is subdivided into anterior (aSPCs, purple) and posterior (pSPCs, orange) SPCs. Future neural crest cells (NCC, dark grey) occupy the territory between the neural plate and pSPCs. The lateral head mesoderm (lHM, green) emerges from the primitive streak and comes to underlie pSPCs, while the prechordal mesendoderm (pME, green) is located in the midline to underlie aSPCs. (b) Diagram of a 10ss embryo. Precursors for different placodes have largely segregated from each other. The olfactory territory (purple) lies in the ectoderm surrounding the anterior forebrain. The trigeminal placode (blue) occupies a broad region next to the midbrain, while the otic placode (salmon) is located next to the hindbrain. The three epibranchial placodes (geniculate, petrosal, nodose; light orange) lie lateral to the otic placode and the paratympanic placode (yellow) is closely associated to the geniculate placode. Note: there are currently no fate maps to ascertain the precise position of paratympanic precursors. (c) Position of placodes at the 25–30ss and their derivatives at later stages.
Figure 2. Gene expression in sensory progenitor cells. The left image shows sensory progenitor cells (SPCs) in a 2ss chick embryo labelled by the expression of Eya2. SPCs surround the neural plate (NP). The nonneural ectoderm (NNE) occupies the ectoderm lateral to SPCs. Right: diagram of an embryo of the same stage; bars at the bottom show the pre‐neural genes are expressed strongly in the neural plate (blue), but at lower level in SPCs (purple), while nonneural genes (red) are strongly expressed in the lateral ectoderm and weakly in SPCs.
Figure 3. Subdividing the pre‐placodal region. (a) Diagram of a 0ss embryo. Anterior SPCs (aSPCs) are induced by signals from the prechordal mesendoderm (pME) including FGF and somatostatin (SST) together with BMP and Wnt antagonists. sSPCs themselves express Nociceptin, which maintains aSPC character in an autocrine manner. Posterior SPCs (pSPCs) are induced by activation of the FGF pathway and inhibition of BMP and Wnt signalling from the lateral head mesoderm (lHM). (b) Differential gene expression along the rostro‐caudal axis of the pre‐placodal territory. At gastrula stages, Otx2 is expressed in aSPCs, while pSPCs express Gbx2. Expression domains overlap at the boundary. At the 1ss stage, Otx2 and Gbx2 domains are more restricted, while additional transcription factors have begun to be expressed in regionally restricted manners. By the 5–9ss, different Pax genes are expressed along the anterior–posterior axis of the pre‐placodal region demarcating precursors for different placodes.
Figure 4. Placode inducing signals. Localised sources of signals induce different placodes from SPCs.
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Buzzi, Ailin L, Hintze, Mark S, and Streit, Andrea(May 2019) Development of Neurogenic Placodes in Vertebrates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027700]