Neural crest and placode interaction during the development of the cranial sensory system

Abstract

In the vertebrate head, the peripheral components of the sensory nervous system are derived from two embryonic cell populations, the neural crest and cranial sensory placodes. Both arise in close proximity to each other at the border of the neural plate: neural crest precursors abut the future central nervous system, while placodes originate in a common preplacodal region slightly more lateral. During head morphogenesis, complex events organise these precursors into functional sensory structures, raising the question of how their development is coordinated. Here we review the evidence that neural crest and placode cells remain in close proximity throughout their development and interact repeatedly in a reciprocal manner. We also review recent controversies about the relative contribution of the neural crest and placodes to the otic and olfactory systems. We propose that a sequence of mutual interactions between the neural crest and placodes drives the coordinated morphogenesis that generates functional sensory systems within the head.

Keywords: Cell fate; Cell migration; Cell movements; Morphogenesis; Sensory nervous system.

Fig. 1

The neural crest (green) migrates in three main streams: the branchial, hypoid and mandbular neural crest streams. In addition, a fourth population migrates into the frontal-nasal region of the head. A subset of cranial placodes that is discussed in the text is shown in red. Roman numerals are used to number pharyngeal arches. Rhombomeres are numbered r1–r8.

Fig. 2

Neural crest and placode cells are closely associated in both the posterior (B–D) and anterior (E–G) head region. (A) Neural crest (green) and placodes (red) arise from adjacent domains within the neural plate border. (B) Neural crest cells of the hyoid and branchial streams migrate around the otic placode and in between the epibranchial placodes as they invade pharyngeal arches II–IV. (C) Neuroblasts from the epibranchial placodes delaminate and migrate along the neural crest to form the cranial ganglia. (D) Joint contribution of neural crest and placodal cells to the epibranchial ganglia. (E) Neural crest migrating into the frontal-nasal region migrate around the developing eye and olfactory placode. (F) GnRH-1 cells delaminate from the olfactory placodes. (G) Neural crest cells provide olfactory ensheathing cells to the placode derived olfactory nerve.

Fig. 3

Chase and run between neural crest and placode cells drives coordinated migration of adjacent cell populations. (A) The placode cells (red) release the chemoattractant Sdf-1 and attract the CXCR-4 expressing neural crest cells (green). (B) Upon contact between the two cell types, N-cadherin dependent junctions form together with an activation of the PCP pathway. These leads to a loss of focal adhesions in the region of contact and a redistribution of forces. (C) As a consequence the placode cells migrate away from the neural crest, which is in turn continually attracted by SDF1.