Dissecting the neural divide: a continuous neurectoderm gives rise to the olfactory placode and bulb

Abstract

The olfactory epithelia arise from morphologically identifiable structures called olfactory placodes. Sensory placodes are generally described as being induced from the ectoderm suggesting that their development is separate from the coordinated cell movements generating the central nervous system. Previously, we have shown that the olfactory placodes arise from a large field of cells bordering the telencephalic precursors in the neural plate, and that cell movements, not cell division, underlie olfactory placode morphogenesis. Subsequently by image analysis, cells were tracked as they moved in the continuous sheet of neurectoderm giving rise to the peripheral (olfactory organs) and central (olfactory bulbs) nervous system (Torres-Paz and Whitlock, 2014). These studies lead to a model whereby the olfactory epithelia develop from within the border of the neural late and are a neural tube derivative, similar to the retina of the eye (Torres-Paz and Whitlock, 2014; Whitlock, 2008). Here we show that randomly generated clones of cells extend across the morphologically differentiated olfactory placodes/olfactory bulbs, and test the hypothesis that these structures are patterned by a different level of distal-less (dlx) gene expression subdividing the anterior neurectoderm into OP precursors (high Dlx expression) and OB precursors (lower Dlx expression). Manipulation of DLX protein and RNA levels resulted in morphological changes in the size of the olfactory epithelia and olfactory bulb. Thus, the olfactory epithelia and bulbs arise from a common neurectodermal region and develop in concert through coordinated morphological movements.

Intertissue mechanical interactions shape the olfactory circuit in zebrafish

“…OP morphogenesis thus represents a relevant in vivo model to investigate the mechanotransduction mechanisms by which neurons sense and transduce extrinsic forces into axon elongation, and in particular where and how novel material (membrane, cytoskeleton) is added along the axon shaft to accommodate stretchinduced growth. Mechanotransduction pathways can also drive changes in cell fate [81][82][83] and could, in the OP, influence neurogenesis and neuronal differentiation, which are concomitant with OP morphogenesis 27,29,37,84 .…”

Building the Border: Development of the Chordate Neural Plate Border Region and Its Derivatives

“…Why do the most anterior regions of the neural plate not generate neural crest? The olfactory placode is derived from the anterior neural fold (Couly and Le Douarin, 1985) which contains multipotent progenitors able to form epidermis, the olfactory placode and the olfactory bulb, and forebrain (Bhattacharyya and Bronner, 2013;Torres-Paz et al, 2020), but not neural crest cells. However, the anterior neural fold has transient competence to generate at least some neural crest, as grafting the chick anterior neural fold to the rostral hindbrain produces migratory neural crest.…”

The Olfactory Tract: Basis for Future Evolution in Response to Rapidly Changing Ecological Niches

“…Previously we have shown in zebrafish that olfactory placodes arise from a large field of neurectodermal cells continuous with the telencephalic precursors in the neural plate and that cell movements, not cell division, underlie olfactory placode morphogenesis (Whitlock and Westerfield, 2000 ; Whitlock, 2008 ). These studies lead to a model whereby a continuous neurectoderm generates both the OBs and olfactory placodes, thus coordinating peripheral OSNs and their central targets during developmental and evolutionary time (Torres-Paz and Whitlock, 2014 ; Torres-Paz et al, 2021 ). This suggests that when faced with external selective pressures, adaptive responses would act on the OSNs and their central synaptic targets as a single developmental and functional unit.…”