NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.

Park BY, Saint-Jeannet JP. Induction and Segregation of the Vertebrate Cranial Placodes. San Rafael (CA): Morgan & Claypool Life Sciences; 2010.

Cover of Induction and Segregation of the Vertebrate Cranial Placodes

Induction and Segregation of the Vertebrate Cranial Placodes.

Show details


During evolution the vertebrate head has acquired a number of unique characteristics, including an advanced craniofacial skeleton and specialized paired sensory organs. These important innovations accompanied the transition of vertebrate ancestors from small filter feeders to large active predators (Northcutt and Gans, 1983). Head skeleton and sensory ganglia originate from two embryonic structures: the neural crest and the cranial placodes. Neural crest and placodes share a number of important features pointing to a possible common evolutionary origin (Schlosser, 2008). They both arise from the neural plate border, boundary between the non-neural ectoderm and the neural plate; they delaminate from the epithelial structure from which they originate; and they have the ability to differentiate into a large array of cell types including sensory neurons, neuroendocrine cells, glia and supporting cells (Baker and Bronner-Fraser, 2001). However, the neural crest has also a set of very unique characteristics that clearly separates it from cranial placodes. Neural crest will develop a much broader repertoire of cell types compared to placodes, including pigment cells, cartilage and smooth muscle cells, and will migrate over greater distances in the embryo. Moreover unlike cranial placodes neural crest are not restricted to the head region, they arise from the entire length of the neural tube starting from a region posterior to the prospective diencephalon. Additionally, while neurons of cranial ganglia have a mixed origin from both neural crest and placodes, the peripheral ganglia in the trunk are exclusively neural crest derived (reviewed in Le Douarin et al., 1986; Baker and Bronner-Fraser, 2001).

Ectodermal placodes are transient thickenings of the embryonic head ectoderm. The term placodes also applies to developing organs such as teeth, mammary glands, hair follicles, feathers and scales, however here we will deal only with placodes that develop in the head and that form part of the sensory nervous system. This includes the adenohypophyseal, olfactory, lens, trigeminal, profundal, otic, epibranchial and lateral line placodes. In most vertebrates development of cranial placodes is initiated shortly after gastrulation when a pre-placodal field of naive ectoderm is established at the border between the future epidermis and the anterior neural plate/neural crest forming regions. According to their location along the anteroposterior axis and the influence of neighboring tissues each placode will adopt a specific identity (Figure 1). It is also important to emphasize that placodes are not merely recipients of inducing signals, and once specified, they are in turn essential for normal development of surrounding structures. For example, the lens is essential for the normal development of the adjacent structures, the retina, iris and overlying cornea; the olfactory placode is required for normal forebrain development; and the otic epithelia induce chondrogenesis in the surrounding mesenchyme, which will provide the protective and structural capsule to the inner ear.

Figure 1. Fate map of cranial placodes at the anterior neural plate.

Figure 1

Fate map of cranial placodes at the anterior neural plate. (A) Schematic representation of a Xenopus laevis embryo at the neurula stage. The pre-placodal ectoderm abuts the neural plate anteriorly and is located lateral to the neural crest. (B) The pre-placodal (more...)

Cranial placodes include rather different structures, probably with different evolutionary origins. While some sensory placodes (otic and olfactory) may have homologues in basal chordates (Wada et al., 1998), the so-called neurogenenic placodes (trigeminal, otic, lateral line and epibranchial placodes) appear to have emerged at a later time (Shimeld and Holland, 2000). Generation of individual neurons from the ectoderm is a character shared by primitive chordates, therefore it is not the neurogenic potential of the ectoderm that is a vertebrate novelty, but more the concentration of foci of neurogenesis (ganglia) in discrete regions of ectoderm (Shimeld and Holland, 2000).

With the exceptions of the lens and the adenohypophyseal placodes, all cranial placodes will give rise to neurons in addition to other cell types. Neurogenic placodes contribute sensory neurons to cranial ganglia and may themselves be divided into two groups based on their location and fate (reviewed in Webb and Noden, 1993; Northcutt, 1996). Dorsolateral placodes (trigeminal, otic and lateral line) occupy relatively dorsal positions adjacent to the hindbrain and give rise to sensory cells of the inner ear and lateral line system, to the sensory neurons of the otic and lateral line ganglia supplying them, and to neurons of the trigeminal ganglion (among other cell types). Epibranchial placodes (geniculate, petrosal, and nodose) lie more ventrally, and are associated with the dorsocaudal aspect of the pharyngeal clefts and give rise to viscerosensory neurons of the facial, glossopharyngeal, and vagal nerves.

In recent years the development of the cranial placodes has been the object of a renewed interest, coinciding with the characterization of new molecular tools to identify placodes at various stages of development. This effort has led to a better understanding of their induction and diversification at the cellular and molecular levels, and has helped establish a draft of the gene regulatory network underlying placode formation. In the last 10 years a number of excellent reviews have discussed and reviewed some of the progress made in the field (Baker and Bronner-Fraser, 2001; Begbie and Graham, 2001; Streit, 2004; 2007; Battacharrya and Bronner-Fraser, 2004; Schlosser and Ahrens, 2004; Brugmann and Moody, 2005; Schlosser, 2005; 2006, 2007, 2008; Bailey and Streit, 2006; McCabe and Bronner-Fraser, 2009; Ladher et al., 2010). Here after a general overview of the development of the different placodes and their derivatives, we will summarize recent advances in characterization of the repertoire of transcription factors underlying placode development. We will also review recent studies beginning to address the role of several classes of signaling molecules in the induction and segregation of cranial placodes from a common pre-placodal region.

The cranial placodes are localized ectodermal thickenings that develop by apicobasal elongation of cuboidal cells in the inner layer of the ectodem in the head of vertebrate embryos. They are involved in formation of sense organs (eye, nose, ear) and cranial sensory ganglia. Despite being grouped under the same term of “ectodermal placodes,” and developing from the same initial territory, they differ greatly in their pattern of development as well as in the derivatives and cell types they generate. There are two major ways in which the placodal ectoderm will be converted into a specific derivative: either by invagination of the thickened epithelium into a vesicle that will separate for the surface ectoderm, or by delamination of cells from the thickened ectoderm and reaggregation in the underlying tissues (Figure 2). Delamination of cells is also occurring in placodal tissue forming by invagination with the exception of the lens. The resulting structures will undergo extensive proliferation and remodeling to give rise to very diverse cell types characteristic for each placodal derivative.

Figure 2. Schematic representation of the early morphogenetic processes associated with the development of the cranial placodes.

Figure 2

Schematic representation of the early morphogenetic processes associated with the development of the cranial placodes. All cranial placodes develop from a thickening of the head ectoderm. Adenohypophysis, olfactory epithelium of the nose, lens, and inner (more...)

Six types of cranial placodes exist in higher vertebrates: 1) the adenohypophyseal placode forming the anterior lobe of the pituitary gland; 2) the olfactory placode that will give rise to the olfactory epithelium of the nose; 3) the lens placode that will differentiate into the transparent lens; 4) the trigeminal placode from which the sensory neurons of the ophthalmic and maxillomandibular lobes of the ganglion of the Vth cranial nerve originate; 5) the otic placode producing precursors for the sensory epithelia of the inner ear and neurons of the VIIIth cranial nerve; and finally, 6) the epibranchial placodes (geniculate, petrosal and nodose) that will produce the sensory neurons for the distal portion of the ganglia of the VIIth, IXth and Xth cranial nerves (the proximal neurons are derived from the neural crest). Fish and amphibians possess an additional placode, known as the lateral line, involved in the mechanosensory detection of water movements and electric fields. Finally, some amphibian species appear to have retained a primitive form of sensory placode known as the hypobranchial placode. Here we provide an overview of the development of each placode and the derivatives they will form.

Adenohypophyseal placode

The pituitary gland or hypophysis is the regulatory center of growth, metabolism and reproduction, and acts as a relay between the hypothalamus and various organs. In most vertebrates the pituitary gland is formed of two distinct parts, an anterior and a posterior lobe known respectively as adenohypophysis and neurohypophysis. The adenohypophyseal placode forms the anterior lobe of the pituitary gland and gives rise to the endocrine secretory cells of the pituitary (reviewed in Asa and Ezzat, 2004), containing five hormone producing cell types: lactotropes (prolactin), gonadotropes (luteinizing hormone and follicle stimulating hormone), thyrotropes (thyroid stimulating hormone), corticotropes (adenocorticotropic hormone) and somatotropes (growth hormone).

Fate-mapping studies in amphibian, chick and mouse embryos (Eagleson et al., 1986; 1995; Couly and Le Douarin, 1985; Cobos et al., 2001; Osumi-Yamachita et al., 1994; Kawamura et al., 2002) have shown that the cells contributing to the adenohypophysis develop at the midline of the anterior neural ridge, which delineates the rostral boundary of the neural plate, a region devoid of neural crest. The anterior neural ridge also gives rise to the olfactory placodes and some forebrain tissues including the olfactory bulbs (reviewed in Papalopulu, 1995). Ablation of this region in chick embryos at the 2-4 somite stage confirmed these lineage analyses as it prevented formation of Rathke’s pouch and any further pituitary development (elAmraoui and Dubois, 1993). Upon head folding, the oral ectoderm cells of the adenohypophyseal placode invaginate towards the prospective ventral diencephalon to form Rathke’s pouch, the anlage of the adenohypophysis. Rathke’s pouch starts as an invagination of the oral ectoderm in response to inductive signals from the prospective diencephalon. The region of the diencephalon above the pouch is known as the infundibulum and forms the posterior lobe of the pituitary or neurohypohysis (Figure 3). While in most basal fish and tetrapods the adenohypophyseal anlagen invaginates to form Rathke’s pouch, in teleost fish the adenohypophyseal placode does not invaginate but rather maintains its initial organization forming a solid structure in the head (reviewed in Pogoda and Hammerschmidt; 2009).

Figure 3. Development of the adenohypophysis.

Figure 3

Development of the adenohypophysis. (A) Schematic representation of a sagittal section through the stomodeum of an early mouse embryo. The boxed area corresponds to the region from which the future adenohypophysis will develop as shown in subsequent panels. (more...)

The sequence of events leading to pituitary formation is especially well described at the cellular and molecular levels in the mouse embryo (reviewed in Burgess et al., 2002; Rizzoti and Lovell-Badge, 2005). In the mouse, the first sign of pituitary development occurs at 7.5 days post coitum (dpc) with the thickening of the ectoderm at the midline of the anterior neural ridge forming the adenohypophyseal placode. As development proceeds, the anterior neural tube bends and rapidly expands, displacing the adenohypophyseal placode ventrally, within the ectoderm at the roof of the future oral cavity. Around 9 dpc, the placode forms an invagination, the rudimentary Rathke’s pouch. Then, a restricted region of the prospective ventral diencephalon above the pouch gives rise to the infundibulum from which the posterior pituitary or neurohypohysis forms. The close juxtaposition of Rathke’s pouch and the diencephalon is required for tissue interactions between neural and oral ectoderm. By 10.5 dpc, the pouch is fully developed, and at 12.5 dpc it is completely detached from the oral ectoderm and becomes intimately associated with the neurohypohysis. Further shaping and branching of Rathke’s pouch into the mature adenohypohysis varies greatly between species.

Olfactory placodes

The olfactory system transduces signals from the outside world through a group of sensory neurons (olfactory receptor neurons) whose axons project directly into the olfactory bulb. The olfactory epithelium harboring these neurons line the dorsal roof, septum and lateral turbinates of the caudal region of the nasal cavity, and is derived from the olfactory placodes. As for the adenohypohyseal placode, classical transplantation and cell labeling experiments in the chick, Xenopus and zebrafish embryos indicate that the olfactory placodes arise from the anterior neural ridge, from two areas lateral to the adenohypohyseal anlagen (Couly and Le Douarin, 1985; Eaglson et al., 1995; Kozlowski et al., 1997).

In Xenopus as the neural plate closes to form the neural tube the anterior neural ridge coalesces to form an outer epithelial structure known as the “sense plate” (Figure 4). At the tailbud stage the olfactory placodes start to thicken and differentiate as two bilateral areas within the sense plate. At this stage, the sense plate is composed of two cell layers, which will both contribute distinct cell types to the olfactory epithelium (Klein and Graziadei, 1983; Burd, 1999). In most vertebrates the olfactory placodes invaginate to form the epithelia of the olfactory organ, which is odor-sensing and the vomeronasal organ mainly used to detect pheromones (reviewed in Buck, 2000). Some amphibians develop an additional cavity, known as the middle cavity, which often occurs de novo at metamorphosis (Figure 4). This cavity is lined with an olfactory epithelium specifically involved in the detection of water-borne odorants (Higgs and Burd, 1999; Taniguchi et al. 2008). In all species the epithelium of the olfactory organs contain ciliated olfactory neurons, harboring receptors responding to odor-producing substances dissolved in the serous layer covering the epithelium, supporting cells and basal cells (Farbman, 1994). The basal cells are stem cells of the olfactory epithelium that have the ability to divide and continuously produce new neurons during embryogenesis and throughout the adult life of the organism. The axons of the sensory neurons project to the olfactory bulb forming the olfactory, vomeronasal and terminal nerves.

Figure 4. Development of the olfactory placode in the frog Xenopus laevis.

Figure 4

Development of the olfactory placode in the frog Xenopus laevis. (A) Frontal views of Xenopus embryos showing the position of the anterior neural ridge (stage 14), the sense plate (stage 20) and the olfactory placodes (stage 32). Modified from Drysdale (more...)

The olfactory placodes also give rise to glial cells that ingress and migrate along the olfactory nerve towards the brain (Ramon-Cueto and Avila, 1998). Olfactory placodes are the only ectodermal placodes to produce glia, a cell type typically derived from neural crest (Couly and LeDouarin, 1985; Baker and Bronner-Fraser, 2001). The olfactory placodes are also producing gonadotropin-releasing hormone (GnRH) neurons that migrate along the olfactory and vomeronasal nerves into the brain (reviewed in Wray, 2002). GnRH neurons project their axons in different regions of the brain, which have been implicated in the control of some aspects of reproduction. Recent lineage tracing experiments in zebrafish challenged this view, suggesting that GnRH neurons may in fact originate from the neural crest and the adenohypophyseal placode (Whitlock et al., 2003; reviewed in Whitlock, 2005).

Lens placodes

Historically, lens induction has been a preferred model for studying inductive interactions during embryogenesis. Classical transplantation experiments using amphibian embryos suggested that the optic vesicle is the source of lens-inducing signals sufficient to generate lens tissues in competent ectoderm (reviewed in Grainger et al., 1996). More recent findings suggest a multistep model for lens induction. There is now good evidence that lens specification occurs at the neurula stage, before the optic vesicle contact the surface ectoderm, and that neural crest cell migration in the frontonasal region is required to restrict the position of the lens placode (Bailey et al., 2006).

Development of the lens is closely linked to morphogenesis of the eye and depends on mutual interaction between the optic cup and the lens vesicle. These processes have been well characterized at the cellular and molecular levels, with one key master regulator, the transcription factor Pax6, which is both necessary and sufficient for eye development throughout the animal kingdom (reviewed in Ogino and Yasuda, 2000; Chow and Lang, 2001; Lang, 2004; Donner and Mass, 2004). The first morphological indication of eye formation is a bilateral outpocketing of the wall of the diencephalon. These outpocketings deepen to form the primary optic vesicle that will extend toward and contact the surface ectoderm to induce thickening of the prospective lens placode. The optic vesicle progressively bends around the lens placode, forming the bilayered optic cup. The optic cup will differentiate into two layers. The outer layer produces melanin pigment and ultimately becomes the retinal pigmented epithelium. Cells of the inner layer proliferate rapidly and generate a variety of ganglion cells, glia, interneurons and light sensitive photoreceptors neurons. Collectively, these cells constitute the neural retina. As the cavity of the optic cup deepens, the lens placode invaginates into the cup to form an open lens vesicle. Eventually the lens vesicle closes and breaks away from the superficial ectoderm to constitute a rounded epithelial body lying inside the optic cup (Figure 5).

Figure 5. Development of the lens placode into the mature lens.

Figure 5

Development of the lens placode into the mature lens. Diagrams illustrating the sequence of events leading to formation of the lens in a vertebrate embryo. The presumptive lens placode ectoderm is in direct contact with the optic vesicle. The ectoderm (more...)

Differentiation of the lens into a transparent structure with the appropriate optical qualities involves a complex sequence of events culminating in the synthesis of a class of lens-specific proteins known as crystallins. This process involves a regulatory pathway that is both complex and evolutionary conserved (reviewed in Reza and Yasuda, 2004; Lovicu and McAvoy, 2005). Initially the posterior cells of the lens elongate to form the primary lens fibers while the anterior cells retain a low cuboidal configuration. This process reduces the original cavity of the lens vesicle to a slit. The transformation from epithelial cells to lens fibers takes place within a domain at the equator of the lens. Adjacent to this domain is a germinative region of dividing cells. These cells progressively move into the equatorial zone where they stop dividing to initiate elongation and differentiation.

Profundal/trigeminal placodes

The trigeminal ganglion complex of cranial nerve V innervates much of the head. This ganglion develops from two separate ganglia, the ophthalmic and maxillomandibular (reviewed by Baker and Bronner-Fraser, 2001). In anamniotes, the ophthalmic and maxillomandibular lobes of the trigeminal complex are referred as the profundal and trigeminal placodes, respectively. In most organisms the two ganglia fuse during embryogenesis into a single unit. In Xenopus, the profundal and the trigeminal ganglia are separate distally but fused at their proximal end as they condense around stage 24 (Schlosser and Northcutt, 2000). In fish, frogs, birds, and mice the profundal /trigeminal or ophthalmic/maxillomandibular placodes contribute cutaneous sensory neurons to their respective ganglia in a similar manner (Schilling and Kimmel, 1994; Schlosser and Northcutt, 2000; Hamburger 1961; D’Amico-Martel and Noden, 1983; Ma et al., 1998). These neurons extend peripheral axons underneath the skin of the head, to detect mechanical, chemical, and thermal stimuli, and central axons into the hindbrain, to communicate these inputs to the central nervous system. In mammals, the ophthalmic branch of the trigeminal ganglion complex innervates the skin of the head region, the eyeball and eye muscles, and the nose; the maxillary branch innervates the upper jaw, while the mandibular branch innervates the lower jaw and tongue (Baker and Bronner-Fraser, 2001).

The profundal/trigeminal placodes are positioned halfway between the prospective eye and ear, adjacent to the future midbrain-hindbrain boundary. Factors secreted by the dorsal neural tube are implicated in trigeminal placode induction (Stark et al., 1997; Baker et al., 1999). As recently described in zebrafish the sensory neurons are typically born as scattered cells delaminating from placodal tissue and accumulating in the underlying mesenchyme. These neurons eventually coalesce to form a compact cluster of cells (Knaut et al., 2005). Transplantion experiments in chick embryos have shown that the trigeminal ganglion has a mixed origin. It contains neurons from both the neural crest and from placodes, with glial cells and all supporting cells entirely derived from the neural crest (Figure 6; Hamburger, 1961; Narayanan and Narayanan, 1978; Ayer-Le Lievre and Le Douarin 1982; D’Amico-Martel and Noden, 1983). This dual contribution extends to most organisms. In Xenopus, neural crest cells appear to join the cells aggregating under the placodal region at stage 21, however there is no direct evidence that this neural crest contribution applies equally to both ganglia of the trigeminal complex (Schlosser and Northcutt, 2000).

Figure 6. Trigeminal and epibranchial placodes contribution to sensory neurons in the chick embryo.

Figure 6

Trigeminal and epibranchial placodes contribution to sensory neurons in the chick embryo. Sensory ganglia and the placodes from which they arise are color-coded on this diagram of a chick embryo. The position of the trigeminal and epibranchial placodes (more...)

Otic placodes

The inner ear is the organ responsible for hearing, balance and detection of acceleration, and it is almost entirely derived from the otic placode. With the exception of the pigment cells of the stria vascularis and the secretory epithelium of the cochlea, which are of neural crest origin, all components of the inner ear derive from the otic placode (reviewed in Torres and Giraldez, 1998; Fekete and Wu, 2002; Noramly and Grainger, 2002; Whitfield et al., 2002; Riley and Phillips, 2003, Barald and Kelley, 2004).

In most species the thickening of the ectoderm into a placode occurs in a region adjacent to rhombomere 5 (reviewed in Ohyama et al., 2007), while in amphibians the otic placode is centered onto rhombomere 4 (Ruiz i Altaba and Jessell, 1991). Transplantation and ablation experiments suggest that otic placode induction depends on signals derived from surrounding tissues, the prospective hindbrain and the head mesoderm. However, the relative importance of these inducing tissues differs from one species to another (reviewed in Jacobson, 1966; Torres and Giráldez, 1998; Baker and Bronner-Fraser, 2001; Noramly and Grainger, 2002; Riley and Philipps, 2003; Ohyama et al., 2007). For example, in zebrafish grafting hindbrain tissue on the ventral side of an embryo induces ectopic otic vesicles (Woo and Fraser, 1998). Mutations disrupting formation of the prechordal plate and paraxial head mesoderm delay, but do not prevent otic placode induction in zebrafish (Mendonsa and Riley, 1999). In the chick, removal of paraxial head mesoderm underlying the presumptive otic ectoderm prevents otic placode development, even when replaced by mesoderm from a different origin (Kil et al., 2005). In Xenopus prospective hindbrain-derived signals are sufficient to initiate otic development in the absence of mesoderm cues (Park and Saint-Jeannet, 2008).

Once specified, the otic placode invaginates to form an otic cup, which eventually separates from the surface ectoderm to form the otic vesicle or otocyst, a rounded structure without apparent polarity (Figure 7). As the otic placode invaginates into a cup neuroblasts delaminate from the anterior ventral aspect of the otic epithelium to give rise to neurons of the vestibulocochlear (statoacoustic) ganglion of cranial nerve VIII. This ganglion will provide afferent innervation for hair cells associated with both the auditory and vestibular components of the inner ear (Figure 7). Differential rates of cell division and complex morphogenetic movements will shape the otic vesicle into a highly specialized and asymmetrically organized structure.

Figure 7. Development of the otic placode into the inner ear.

Figure 7

Development of the otic placode into the inner ear. Diagrams illustrating the development of the inner ear in a vertebrate embryo. Formation of the otic placode by thickening of the ectoderm adjacent to the prospective hindbrain. The placode invaginates (more...)

The vertebrate otocyst can be divided into two functional domains along its dorsoventral axis: the ventral region is responsible for the sense of hearing, and the dorsa region is involved in vestibular functions. In the mature inner ear, the utricle and semicircular canals constitute the vestibular apparatus. Structurally and functionally these elements are highly conserved in vertebrates. In contrast, the ventrally located auditory chambers have undergone more extensive evolutionary modifications. The saccule and lagena are prominent auditory organs in fish but the saccule has a vestibular role in mammals and birds, and the lagena is absent in mammals. The primary auditory organ in mammals and birds is the cochlea, which has no known counterpart in amphibians and fish (Riley and Phillips, 2003). In amphibians, the saccule, the basilar papilla and the amphibian papilla assume auditory function. In this organism the saccule is a low-frequency vibration/sound detector, while the amphibian papilla and basilar papilla, are low- to mid-frequency and high-frequency sound detectors, respectively (Smotherman and Narins, 2000).

Each chamber is associated with a sensory epithelium containing support cells and mechanosensory hair cells, which convey auditory and vestibular information. The maculae are the sensory epithelia of the utricle (utricular macula) and saccule (saccular macula). The sensory epithelia associated with each semicircular canal, known as anterior, horizontal and posterior cristae, are sensitive to fluid motion caused by angular acceleration. The sensory epithelia in the utricle, saccule and lagena, are associated with otoliths or otoconia (small crystals of calcium carbonate), which facilitate vestibular and auditory function by transmitting accelerational forces and sound vibrations, respectively, to mechanosensory hair cells (reviewed in Fritzsch et al., 2002; Barald and Kelley, 2004; Fritzsch et al., 2006).

Epibranchial placodes

The three epibranchial placodes are located ventral to the otic placode, and dorsocaudal to the pharyngeal clefts, which separate each pharyngeal (branchial) arch. Epibranchial placodes-derived neurons innervate internal organs to transmit information such as heart rate, blood pressure, and visceral distension from the periphery to the central nervous system (Baker and Bronner-Fraser, 2001). From rostral to caudal the epibranchial placodes comprise the geniculate, petrosal, and nodose placodes, each associated in sequence with the first, second and third branchial clefts. Each placode contributes sensory neurons to cranial nerves VII (facial nerve), IX (glossopharyngeal nerve), and X (vagal nerve), respectively (Figure 6). More specifically, epibranchial placodes contribute viscerosensory neurons solely to the distal ganglia of cranial nerves VII, IX and X, innervating several visceral organs and the taste buds (reviewed in Northcutt, 2004). The proximal ganglia of cranial nerves VII, IX and X are derived from neural crest and produce somatosensory neurons (Narayanan and Narayanan, 1980; Ayer-Le Lievre and Le Douarin; 1982; D’Amico-Martel and Noden, 1983). While the distal (placodally-derived) and proximal (neural crest-derived) ganglia of cranial nerves VII, IX, and X are clearly distinct in amniotes, they cannot be distinguished in Xenopus due to the early fusion of the ganglion primordia (Schlosser and Northcutt, 2000). In a very detailed analysis, Schlosser and Northcutt have shown that during Xenopus development, the facial ganglion is intimately fused with the anteroventral lateral line ganglion, while the glossopharyngeal ganglion is fused with the middle lateral line ganglion (Schlosser and Northcutt, 2000). Fish and amphibians form additional vagal epibranchial placodes associated with more posterior branchial clefts. For example three vagal epibranchial placodes have been described in Xenopus (Schlosser and Northcutt, 2000) and six in the lamprey (Damas, 1951).

Differentiation occurs by delamination of cells from the thickened placode, similar to what is seen for the trigeminal and lateral line placodes (Figure 2). Delaminated neuroblasts then coalesce to form ganglia that make appropriate connections to their targets. Early work in the chick embryo suggested that these placodes were induced by signals derived from adjacent tissues including the cranial neural crest and the pharyngeal endoderm (Webb and Noden, 1993). However, later ablation experiments have shown that epibranchial placodes can form in the absence of neural crest (Begbie et al., 1999). Recent work in zebrafish indicates that epibranchial placodes induction depends on cranial mesoderm-derived signals that establish both the epibranchial placodes and development of the pharyngeal endoderm, which is subsequently required to promote neurogenesis in the epibranchial placodes (Nechiporuk et al., 2007). Another study suggested that the initial induction of both otic and epibranchial placodes share common signals derived from the hindbrain (Sun et al., 2007).

Development of the otic and epibranchial placodes was long thought to be independent, consistent with the very distinct functions mediated by the inner ear and the epibranchial ganglia. Recent studies indicate that may not be the case. For example cells destined to form the otic and epibranchial placodes are initially intermingled within the pre-placodal ectoderm (Streit, 2002). In addition, recent molecular analyses suggest that epibranchial and otic placodes originate from a common precursor domain defined by Pax2 expression (Sun et al., 2007; reviewed in Ladher et al., 2010). In fact, these properties are also shared by the lateral line placode, suggesting that all three placodes might be developmentally and evolutionary related (Baker et al., 2008).

Lateral line placodes

The lateral line system is an important mechanosensory organ in fish and amphibians and is involved in the detection of water motion and electric fields. It allows for predator and prey detection, object avoidance and social behaviors, such as schooling and sexual courtship (Dijkgraaf, 1963; Montgomery et al., 2000). The lateral line system has completely disappeared in terrestrial tetrapods. The name of “lateral line” comes from the fact that the sensory organs are arranged in lines along each flank on the surface of the body. The lateral line receptor organs include mechanoreceptive neuromasts that respond to disturbances in the water, and in some cases electroreceptive organs that respond to weak electric fields (Webb, 1989). Neuromasts contain a core of mechanosensory hair cells, surrounded by support cells, and are innervated by sensory neurons located in a cranial ganglion (Figure 8A). The neuromasts on the head form the so-called anterior lateral line system, the ganglion of which is located between the ear and the eye, while the neuromasts on the body and tail, including those on the caudal fin, form the posterior lateral line system, its ganglion being just posterior to the ear (Figure 8B). Neuromasts are located either superficially, in shallow dermal pit lines, in cartilaginous grooves, or embedded into bony or cartilaginous canals. Electroreceptors are found either in ampullary or tuberous structures. These ampullary organs are largely restricted to the head while tuberous organs are found in both the head and the trunk. Neuromasts receive afferent and efferent innervation, while electroreceptors are only supplied by afferent fibers (reviewed in Ghysen and Dambly-Chaudiere, 2004; Gibbs, 2004).

Figure 8. Organization of the zebrafish lateral line system.

Figure 8

Organization of the zebrafish lateral line system. (A) Schematic representation of a neuromast. The mechanosensory hair cells are surrounded by support and mantle cells. (B) Schematic representation of an adult fish, illustrating the innervation of the (more...)

Comparative studies of lateral line systems suggest that the lateral line arises from six pairs of lateral line placodes in fish, three located anterior to the otic vesicle (anterodorsal, anteroventral and otic lateral line placodes) and three posterior to the otic vesicle (middle, supratemporal and posterior lateral line placodes). Most amphibians have only five lateral line placodes, due to the loss of the otic lateral line placode, and completely lack electroreceptors (Schlosser and Northcutt, 2000; reviewed in Schlosser, 2002a; 2002b). Each lateral line placode gives rise to a single lateral line nerve that will innervate lateral line hair cells and convey information to the adjacent hindbrain, and to one migrating primordium, which extends and migrates to form the lateral line systems of the head and trunk.

The initial stages of lateral line development from the corresponding placodes have been relatively well described in fish and amphibians (Winklbauer, 1989; Northcutt et al., 1994; Northcutt, 1997; Ledent, 2002; Sarrazin et al., 2010). Briefly, cells delaminating from the thickened placodal epithelium coalese in the underlying mesenchyme to give rise to sensory neurons of the lateral line ganglia, while the remaining placodal cells become lateral line primordia. This primordium elongates or migrates between surface ectoderm and basement membrane in a stereotypical pattern depositing mechanosensory neuromasts at regular intervals. The growth cones of axons of the lateral line ganglion extend along with the primordium, innervating neuromasts as they are deposited. Cephalic lateral line placodes elongate at the rostral end of each placode, whereas the trunk lateral line placodes and their derivatives amigrate caudally along the trunk. The pattern of lateral line distribution and canal branching, and the number of lateral line receptors is species-specific (Northcutt, 1989).

In recent years the development of the lateral line system has been more extensively studied in the zebrafish, an organism highly suitable for live imaging (reviewed in Dambly-Chaudiere et al., 2004; Ghysen and Dambly-Chaudiere, 2004; 2007). More specifically, some of the most recent studies have focused on the signaling pathways (chemokine, fibroblast growth factor, and Wnt) regulating cellular behaviors associated with posterior lateral line migration (Dambly-Chaudiere et al., 2007; Aman and Piotrowski, 2008; Nechiporuk and Raible, 2008; reviewed in Ma and Raible, 2009; Aman and Piotrowski, 2009).

Hypobranchial placodes

A unique type of neurogenic placode known as hypobranchial placodes was recently reported in some amphibian species (Schlosser et al., 1999; Schlosser and Northcutt, 2000; Schlosser, 2003). In Xenopus, these placodes are located ventral and caudal to the second and third pharyngeal pouches and give rise to small hypobranchial ganglia of yet unknown function. They have also been found in another anuran, the direct developing frog Eleutherodactylus coqui (Schlosser, et al., 1999; Scholsser, 2003). Nothing is known about the mechanisms regulating the development of these placodes. Because the development of both epibranchial and hypobranchial placodes arise from a larger placodal domain in the branchial region, it is hypothesized that these newly identified placodes may correspond to ventral extensions of epibranchial placodes (Schlosser, 2003). Neurogenic hypobranchial placodes have not been reported in chick, mouse or zebrafish embryos, raising the possibility that they represent primitive vertebrate characteristics that may have been lost during evolution.

Copyright © 2010 by Morgan & Claypool Life Sciences.
Bookshelf ID: NBK53171


  • PubReader
  • Print View
  • Cite this Page

Other titles in this collection

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...