27.2 Mechanosensory Lateral Line: Microscopic Anatomy and Development

Jacqueline F Webb Department of Biology, Villanova University, Villanova, Pennsylvania, USA

The mechanosensory lateral line system of bony fishes is composed of a series of receptor organs called neuro- masts, which are located on the epithelium or in lateral line canals on the head and trunk (Figure 27.2.1), and are innervated by several lateral line nerves, which project to the hindbrain (see Chapter 15.2).

Structure and function of neuromast receptor organs Neuromast receptor organs are epithelial structures composed of a population of sensory hair cells (which are sensitive to the displacement of their apical ciliary bundles), and nonsensory supporting cells and mantle cells (e.g. Hama and Yamada, 1977; Rouse and Pickles, 1991 a,b).

The apical ciliary bundle of each sensory hair cell is composed of one long kinocilium (with a 9 + 2 microtubule configuration) and a cluster of shorter stereocilia (composed of actin), which are graded in

length and located to one side of the kinocilium (Flock and Wersall, 1962; Flock and Duvall, 1965; Rouse and Pickles, 1991b; Cernuda-Cernuda and Garcia-Fernandez, 1992). Tip links between rows of stereocilia, which have been described in the inner ear of vertebrates, are present in the neuromasts of two species of fishes (Rouse and Pickles, 1991b). The morphology of the kinocilium and stereocilia and

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Figure 27.2.1 Diagrammatic representation of a superficial neuromast (sn) in the epidermis (ep) and a canal neuromast (cn) inside a bony canal (db) in the cyprinid, Hybopsis oestivalis: bm, basement membrane; d, dermis; n, nerve. (From Reno, 1969, reprinted with permission by The American Society of Ichthyologists and Herpetologists.)

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the number of stereocilia in a hair cell vary within and among neuromasts within an individual (e.g. Yamada, 1973; Cernuda-Cernuda and Garcia- Fernandez, 1992), and among species (Popper and Platt, 1993). Hair cell heterogeneity, similar to that found in the auditory system of mammals (e.g. Type I vs. Type II hair cells), has been demonstrated in fishes, based on the differential susceptibility of hair cells in canal and superficial neuromasts to destruction by gentamicin sulfate (Songet al., 1995).

Each hair cell is morphologically polarized as a result of the relative positions of the single kinocilium and the cluster of stereocilia on its apical surface. The morphological polarization of a hair cell defines its axis of best physiological sensitivity to water move- ment (see Chapter 15.2). The physiological properties of mechanosensory hair cells in the lateral line system have only been studied in a few fish species (e.g. Flock and Wersall, 1962; Kroese and van Netten, 1989; van Netten, 1997; Wiersinga-Post and van Netten, 1998). Our knowledge of hair cell physiology is based on extensive work in the auditory system of vertebrates (e.g. Hudspeth, 1983; Corwin and Warchol, 1991; Guth et al., 1998; see Chapter 27.4).

Within a neuromast, hair cells are oriented 180 ~ to one another and occur in an approximately 50:50 ratio (Hama, 1972; Rouse and Pickles, 1991a; Figure 27.2.2), so that each neuromast has a single axis of best physiological sensitivity (but see Shardo, 1996). This is in contrast to the maculae of the otolithic organs of the ear of fishes, which consist of patches of hair cells with either one or two different axes of best physiological sensitivity (Popper and Platt, 1993; see Chapter 15.4). The hair cells of canal neuromasts are oriented parallel to the long axis of the canal so that movement of fluid along the length of the canal can provide an effective mechanical stimulus for the canal neuromast. The axis of best physiological sensi- tivity of superficial neuromasts that occur in linear series, including those that are homologues of canal neuromasts (e.g. pedomorphic canal neuromasts, Webb, 1989b; Northcutt, 1992, 1997; Webb and Northcutt, 1997), tends to be parallel to the line of neu- romasts. In contrast, the orientation of superficial neuromasts that are accessory to a canal tends to be perpendicular to the axis of the canal (e.g. Marshall, 1986; Webb, 1989c), thus adding another axis of best physiological sensitivity to the population of neuro- masts. As a result, the lateral line system can respond to water movements arising from several directions. Superficial neuromasts that do not appear to be acces- sory to a canal occur on both the head and trunk of

Figure 27.2.2 Hair cell distribution and morphology within a neuromast of the coral reef fish, Apogon cyanosoma. (a) Cupula (c) partially covering the neuromast; mantle cells (mc) and hair cells (hc) are evident (scale bar= lOlam). (b) Close-up of the surface of the neuromast showing the oval sensory strip with its population of hair cells, and the mantle cells (mc) that surround the sensory strip and define the outer perimeter of the neuromast (scale bar= 10 ~lm). (c) Close-up of the hair cells of the sensory strip showing the kinocilium (k) and stereocilia (s) of each hair cell. The overall axis of polarization of the hair cell population is represented by arrows (scale bar = 1 ~lm). (From Rouse and Pickles, 1991 b, reprinted by permission of Wiley-Liss, Inc.)

fishes (e.g. Northcutt, 1989; Teyke, 1990; Webb and Northcutt, 1997).

Hair cells are located in a portion of the neuro- mast called the sensory strip, which is typically round, oval or elongated (Figures 27.2.2 and 27.2.3). The sensory strip is surrounded by mantle cells that secrete the cupula (Kelly and van Netten, 1991; Mukai et al., 1991; Rouse and Pickles, 1991b; Mukai and Kobayashi, 1992) in which the ciliary bundles of all of the hair cells are embedded (Figure 27.2.2). The cupula provides a mechanical linkage between the hair cells and the external hydrodynamic environ- ment. The functional significance of heterogeneity

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Figure 27.2.3 Scanning electron micrographs demonstrating morphological variation in neuromasts among teleost fishes. (A) Canal neuromast from the narrow head canal of the sculpin, Cottus bairdi (courtesy of S. Coombs). (B) A superficial neuromast from the trunk of the flatfish, Scophthalmus aquosus (Newman, Chambers and Webb, unpublished data). (C) Canal neuromast from a widened head canal of the blind side of the head in the rex sole, Glyptocephalus sp. (D) Canal neuromast from a widened head canal of the clown knifeflsh, Notopterus chitala (courtesy of S. Coombs). (E) Superficial neuromast from the blind side of the head of the California tongue sole, Symphurus atricauda.

in cupular structure is still unclear (Kelly and van Netten, 1991; Rouse and Pickles, 1991b). The cupula of superficial neuromasts grows continuously (Mukai and Kobayashi, 1992); the height of the cupula of canal neuromasts is limited by canal diameter. The shape of the neuromast generally defines the contour of the perimeter of the cupular base (but preparation artifact is common and cupular morphology is gener- ally hard to discern.

The morphology of canal neuromasts is corre- lated with canal morphology. Neuromasts in narrow canals tend to be oval, with the long axis parallel to the axis of the canal (Figure 27.2.3A). Neuromasts in widened canals are much larger (in some cases, an order of magnitude larger); their hair cells are located in a round or oval sensory strip, but the mantle cells

that surround the sensory strip and define the outer perimeter of the neuromast, span the width of the canal (Coombs et al., 1988; Webb, 1989a; Figure

VI 27.2.3C and D). Superficial neuromasts ( = pit organs, m

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masts within a given individual (M/inz, 1989; "< Wonsettler and Webb, 1997). They are generally "< round or oval, and have a round or narrow and elon- gated sensory strip (Figure 27.2.3B and E). Recently, Marshall(1996) described two new types of superficial "" neuromasts in two species of deep-sea fishes, which m appear to consist only of a very long, thin sensory :1: strip that is located either flat on the skin surface, or =, on the edge of a flap of skin.

The length of kinocilia and stereocilia, number m and density of hair cells, the shape and stiffness of the cupula, and the size and shape of a neuromast all have .~ functional consequences (Denton and Gray, 1989; I "

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1991; van Netten and Khanna, 1994). Interspecific and ontogenetic variation in these parameters need to e- be investigated in order to understand their potential

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1989b, 1999; Northcutt , 1992). Like those of the sensory maculae of the inner ear, O

the hair cells in neuromasts of the lateral line system -< in both fishes and amphibians develop from cranial ectodermal placodes (reviewed by Northcutt, 1992; Webb and Noden, 1993; Northcutt et al., 1994; Figure 27.2.4). Several older studies have provided detailed descriptions of the differentiation of neuromasts and sensory neurons from cranial ectodermal placodes (reviewed by Northcutt, 1992, 1997). More recently, it has been clearly demonstrated in both fishes and especially in amphibians (Fritzsch and Neary, 1998), that several lateral line placodes arise in cranial

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Figure 27.2.4 Ectodermal placodes on the head of the axolotl, an amphibian model system in which lateral line placodes are well known. (a) and (b) The lateral line placodes (black), and other sensory and neurogenic placodes (gray) in stage 35 and stage 37 axolotl embryos. (c) The lateral line placodes in a stage 38 larval axolotl, showing the elongation of placodes on the head and trunk that delineate lines of neuromasts that will differentiate from them: ad, anterodorsal lateral line placode; dtl, dorsal trunk lateral line; fe, facial epibranchial placode; Ip, lens placode, mid, middle lateral line placode; midd, dorsal subdivision of middle lateral line placode, midv, ventral subdivision of middle lateral line placode; mtl, main trunk lateral line; ol, olfactory placode; otv, otic (octaval) vesicle; pld, dorsal subdivision of posterior lateral line placode, plm, main subdivision of posterior lateral line placode; plv, ventral subdivision of posterior lateral line placode; std, dorsal subdivision of supratemporal lateral line piacode; stv, ventral subdivision of supratemporal lateral line placode; st, supratemporal lateral line placode. (From Northcutt et o1., 1994, reprinted by permission of Wiley-Liss, Inc.)

ectoderm and elongate over the head (Northcutt et al.,

1994, 1995; Northcutt, 1997) and down the trunk (Metcalfe et al., 1985; Vischer, 1989; reviewed by Northcutt, 1992, 1997), delineating the lines of neuro- masts that subsequently differentiate in situ (Otsuka and Nagai, 1997; Figure 27.2.4). One recent paper has suggested that, in addition to placodes, neuromasts are partially derived from neural crest cells (Collazo et al., 1994). The sensory neurons that compose the lateral line nerves and innervate the neuromasts (Northcutt et al., 1994; Northcutt and Brandle, 1995; see Chapter 15.2), and the electroreceptor organs (in those species that have them), also differentiate from lateral line placodes (Northcutt et al., 1995; Fritzsch and Neary, 1998).

At hatching, neuromasts generally are present in the epithelium on both the head and trunk (e.g. Blaxter et al., 1983; Blaxter, 1987; Metcalfe, 1989; Blaxter and Fuiman, 1990; Otsuka and Nagai, 1997; Figure 27.2.5). Hair cells of differentiated neuro- masts that are present in embryos and larvae are innervated, and are considered functional (Otsuka and Nagai, 1997). Neuromast number (e.g. Metcalfe, 1989; Vischer, 1989; Harvey et al., 1992) and neuro- mast size (Miinz, 1989; Wonsettler and Webb, 1997; Tarby, 1998) increase, and neuromast and cupular shape change, ontogenetically (e.g. Blaxter et al.,

1983; Miinz, 1986, 1989; Webb, 1989b; Harvey et al.,

1992; Wonsettler and Webb, 1997). Evidence from amphibians demonstrates that neuromast size increases with the addition of hair cells that differenti- ate from support cells, and that hair cells are capable of regeneration (Balak et al., 1990; Corwin and Warchol, 1991; Jones and Corwin, 1996). H air cells in various stages of development are present in neuro- masts, and new hair cells are produced in pairs, with opposite polarities, which may be the result of a single mitotic event (Rouse and Pickles, 1991a). Hair cells have been shown to exhibit turnover within a neuro- mast (Rouse and Pickles, 1991a), but with one known exception (Shardo, 1996), the axis of orientation of the hair cells in a neuromast, and therefore the neuro- mast's axis of best physiological sensitivity, appears not to change ontogenetically (Mi~nz, 1989; Vischer, 1989; Webb, 1989b).

Late during the larval period, or at transformation to the juvenile stage, the lateral line canals form as epithelial ridges begin to rise on either side of a sub- set of individual neuromasts on the head (the pre- sumptive canal neuromasts; M~nz, 1986), making it appear that these neuromasts are sinking between these ridges into epithelial grooves. Intramembranous

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ossification within these ridges forms the canal walls. The ridges fuse over the neuromast and the canal walls extend medially and fuse to form the canal roof (e.g. Webb, 1989c; Tarby, 1998; Figure 27.2.6). The epithelial tissue surrounding and lining adjacent canal segments fuse leaving a common epithelial pore between adjacent canal segments. Intramembranous ossification of canal segments that compose a lateral line canal (e.g. the mandibular canal, see Chapter 15.2) is non-synchronous and non-sequential (Kapoor, 1961; Webb, 1989b,c; Tarby, 1998). After canal segment ossification, the bony walls of adjacent segments fuse and the lateral line canals become inte- grated into the cranial dermal bones forming the 'lateral line bones', which are prominent components of the adult fish skull (e.g. Lekander, 1949; Disler, 1960; Branson and Moore, 1962; Cubbage and Mabee, 1996; Adriaens et al. , 1997; Tarby, 1998; see Chapter 15.2). After canals are formed and integrated into dermal bones, neuromast size and canal diameter continue to increase with fish size (Tarby, 1998). Neuromasts that remain superficial stay relatively small throughout life (M/~nz, 1989) and additional superficial neuromasts may continue to differentiate

and proliferate throughout the larval and juvenile periods.

On the trunk, superficial neuromasts occur in one or more linear series in the epithelium overlying the myomeres of the trunk musculature (Blaxter et al.,

1983; Metcalfe, 1989), and increase in number before a final number of neuromasts is established. The lat- eral line scales develop in the dermis beneath each of the trunk neuromasts, late during the larval stage. Canal morphogenesis is similar to that on the head. Each neuromast becomes enclosed in a canal segment formed by the fusion of two epithelial ridges that rise on either side of the neuromast. A canal segment ossi- fies intramembranously in association with the flat scale beneath it, forming a tubed lateral line scale (Webb, 1989c; Wonsettler and Webb, 1997). Adjacent canal segments are associated with individual scales; the canal lumen is linked by a common epithelial pore, but the ossified walls and roof of adjacent canal segments do not fuse. Canal morphogenesis generally proceeds in a rostal to caudal direction (Vischer, 1989; Webb, 1989a, 1999; Wonsettler and Webb, 1997), resulting in the development of a pored trunk canal that consists of a series of overlapping, tubed

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Figure 27.2.6 Diagrammatic representation of the morphogenesis of the lateral line canals of the head in the cichlid, Archocentrus nigrofasciatus. (a) Stage I - A superficial neuromast (nm) is located in the epidermis (ep) that sits above the basement membrane (bm); underlying dermal bone is present in the dermis. (b) Bony canal walls ossify intramembranously and extend upward from the underlying dermal bone (db) on either side of a neuromast, which appears to sink into an epithelial groove. (c) The epithelium fuses over the neuromast (nm) forming an epithelial canal. (d) The dermal canal bone continues to ossify intramembranously and the canal walls fuse medially to form the canal roof: nm, neuromast; bm, basement membrane; d, dermis; dm, dermal bone; ep, epithelium. (From Tarby, 1998.)

lateral line scales (see Chapter 15.2). Superficial neuro- masts, which are generally smaller than canal neuro- masts may remain in the epithelium in association with the canal (Webb, 1989b,c; Wonsettler and Webb, 1997).

Mechanisms responsible for patterns of develop- ment in the lateral line system of both fishes and amphibians are now being explored using modern approaches in a limited number of model species (see Fritzsch and Neary, 1998). Perturbations of the lateral line system have been observed in zebrafish mutants (e.g. Whitfield et al., 1996; Nicholson et al., 1998). In addition, the distribution pattern of neuromast- specific antigens (Kornblum et al., 1990), expression patterns of HOX genes (Ekker et al., 1997; Metscher et al., 1997), and the role of neural crest in patterning and morphogenesis of the lateral line system (Smith et al., 1988, 1990; Parichy, 1996a,b) have been exam- ined in zebrafish and amphibian model systems. The examination of patterns of gene expression, as well as the nature of tissue interactions during embryogen- esis will shed light on the mechanisms underlying the patterning of neuromast receptors on both the head and trunk of fishes. The nature of the interaction between neuromasts and dermal bone that can account for the pattern of distribution of the lateral line canals in dermal skeletal elements (see Devillers, 1947; DeBeer, 1985) and the mechanisms underlying

the morphogenesis of lateral line canals (see Wonsettler and Webb, 1997, for discussion) are still not fully understood.

Acknowledgments Dr Sheryl Coombs kindly provided two original photos. Ms Melissa Tarby granted permission for the reproduction of an original illustration from her unpublished MS thesis, and Leo Smith assisted in the preparation of figures. Supported by NSF grant IBN 9603896.

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