the laboratory fish || mechanosensory lateral line

15.2 Mechanosensory Lateral Line: Functional Morphology and

; Neuroanatomy , . I

Jacqueline F Webb U1 Department of Biology, Villanova University,

Villanova, Pennsylvania, USA 8 .,Z,

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, ~ , Introduction mechanosensory organs, the vesicles of Savi and the

W spiracular organs, are only found in some groups of non-teleost fishes (Barry and Bennett, 1989;

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The mechanosensory lateral line system is present in all fishes and in most amphibians, but lost in reptiles and their derivatives (Northcutt, 1989). It consists of a series of sensory organs called neuromasts, which are composed of hair cells and are located in lateral line canals, or on the epithelium of the head and trunk of fishes (Coombs et al., 1988; Webb, 1989b). The structure and function of the mechanosensorylat- eral line system has been studied by ichthyologists and physiologists for over a century (reviewed by Dijkgraaf, 1962, 1967, 1989; Hensel, 1978; Coombs et al., 1992), and has been the subject of much more intense study in the past 30 years (Cahn, 1967; Atema et al. , 1988; Coombs et al., 1989).

In living jawless fishes, the hagfishes and lam- preys, the mechanosensory lateral line system is either rudimentary or absent (Northcutt, 1989; Braun, 1996; Braun and Northcutt, 1997). The system is well developed in sharks, skates, and rays (Tester and Kendall, 1967; Northcutt, 1989; Maruska and Tricas, 1998), and in bony fishes (Coombs et al., 1988; Webb, 1989b); it is also present in larval and aquatic adult amphibians (Fritzsch, 1989; Northcutt, 1990; Northcutt et al., 1995). In addition to neuromasts, two other structurally and functionally specialized

Northcutt, 1992), but are also considered to be a part of the lateral line system.

Traditionally, the mechanosensory lateral line system was considered to be a component of an 'acousticolateralis system', which included the auditory system and both the mechanosensory and electrosensory lateral line systems (Plattet al., 1989). However, we now know that several fundamental features distinguish these sensory systems from one another. For instance, the mechanosensory lateral line and auditory systems consist of sensory organs composed of hair cells, but develop from different ectodermal placodes (several dorsolateral placodes, and a single otic placode, respectively; Northcutt, 1992; see Chapter 27.2) and are innervated by different cranial nerves (a series of lateral line nerves, and the auditory nerve (VIII), respectively, Northcutt, 1989). The electrosensory lateral line system is composed of electroreceptors, which develop from the same placodes as the neuromasts and are innervated by branches of the same lateral line nerves that innervate neuromasts (Northcutt et al., 1995). The auditory system and the mechanosensory and electrosensory lateral line systems have distinct central projection patterns (McCormick, 1989) and respond to different

types of stimuli that generally serve different biologi- cal roles (Bodznick, 1989; Kalmijn, 1989, 1997; Coombs et al., 1992).

Morphology of the lateral line system on the head In bony fishes, the lateral line canals are contained in dermal skeletal elements, prominent features of the skull that can be easily observed in dried skeletal mate- rial and in cleared and stained specimens (Webb, 1989b; Cubbage and Mabee, 1996; Adriaens et al.,

1997; Tarby, 1998; Figure 15.2.1). Typically, these cephalic lateral line canals are present in the neuroo cranial bones located above the eye (supraorbital canal), and in the circumorbital bones below the eye (infraorbital canal). A canal runs down the length of the preopercular bone (preopercular canal) and into the bones of the lower jaw to the mandibular symphy- sis (mandibular canal). The head canals generally con- verge in the otic region of the skull where a canal extends dorsally through the extrascapular bones ( = supratemporal commissural canal), and may join the corresponding canal on the opposite side of the head. Finally, a canal generally runs through the post- temporal and supracleithral bones where it joins the trunk canal contained in the lateral line scales. The lateral line canals are lined by a thin epithelium in which neuromast receptor organs are located, and are incorporated into dermal bones, which sit below the basal lamina. In most bony fishes, the lateral line canals are generally well ossified, and are pierced by canal pores, which link the fluid-filled canal lumen with the external environment. The location of the lateral line canals in specific dermal bones of the skull is rather consistent among teleost fishes. Variation in the morphology of the lateral line canals and the bones in which they are contained, and the number and distribution of canal pores on the head, has been used extensively as characters in species descriptions and in phylogenetic reconstructions (Webb, 1989b).

Four general types of cephalic lateral line canal systems have been described among bony fishes: narrow-simple, narrow-branched, reduced, and widened (Figure 15.2.2; reviewed by Webb, 1989b). A narrow- simple canal system is typical of most bony fishes, including experimental model species (Metcalfe,

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Figure 15.2.1 The skull of the cichlid, Archocentrus nigrofasciatus illustrating the location and morphology of the lateral line canals on the head. (a) Lateral view of the skull highlighting the dermal bones containing the lateral line canals: the supraorbital canal in the nasal (na) and frontal (fr) bones, the infraorbital canals in the lacrimal (la) and the infraorbital series (e.g. io), the preopercular canal in the preoperculum (po), the mandibular canal in the dentary (de) and the anguloarticular (aa), the otic canal in the pterotic (pt), the supratemporal commissure in the lateral and medial extrascapulars (le, me), and the post- otic canal in the post-temporal (pe). (b) Dorsal view of neurocranium showing the supraorbital canal (so) in the nasal and frontal bones. (c) Ventrolateral view of mandible showing the mandibular canal (md) in the dentary and anguloarticular bones (from Tarby, 1998).

1989; Puzdrowski, 1989; Cubbage and Mabee, 1996). In these fishes, the canals are well ossified, the canal lumen is generally uniform in diameter, and canal pores appear as holes in the roof of the canal, or as pores at the end of short epithelial tubules that extend from the pore in the canal wall. In a branched canal system (herrings and their relatives, for instance), the bony pores in the canal wall are elongated into bony tubules that are extensively branched and end in numerous terminal pores (Blaxter, 1987). In a reduced canal system, portions of one or more canals are

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Figure 15.2.2 Four types of head canal systems among teleost fishes: (a) narrow-simple canal system; (b) reduced canal system; (c) widened canal system; (d) branched canal system (from Webb, 1989b, reprinted by permission of Karger).

replaced by superficial neuromasts, which may be greatly proliferated (Tekye, 1990; Wongrat and Miller, 1991). In a widened canal system, canal segments are ballooned out with incompletely ossified walls and a canal roof covered by a tympanum-like epithelium. Small canal pores may be present in the epithelium that covers the canals, but these can be easily overlooked and are generally not noted in the description of these canals (J.F. Webb, personal observation). Widened canals are found among a small number of fish families (Webb, 1989b), including many deep sea fishes (Garman, 1899; Marshall, 1996), some flatfishes (Webb, 1988, 1995) and some freshwater fishes (reviewed by Coombs et al. , 1992).

Morphology and distribution of neuromast receptors on the head Neuromast receptor organs are located in epithelial tissue and consist of a population of directionally

polarized hair cells with apical ciliary bundles, surrounded by non sensory supporting cells. The ciliary bundles are embedded in a tall gelatinous cupula (Kelly & van Netten, 1991), which is secreted by the nonsensory cells. Displacement of the cupula, and thus the hair cells, by water flow is the basis for neuromast function (see Chapter 27.2). Neuromasts are distributed in predictable locations within the head canals of fishes (Webb and Northcutt, 1997). However, the distribution of canal neuromasts can only be determined if their location is established in larval stages, before they become enclosed by canals (see Chapter 27.2), or if ossified canals of juveniles or adults are sectioned histologically (Tarby, 1998), or dissected for analysis using scanning electron microscopy. In bony fishes with narrow-simple, or narrow- branched canal systems, canal neuromasts are generally oval in shape with their long axis parallel to the long axis of the roughly cylindrical canal (Coombs et al. , 1988; M/~nz, 1989; Tarby, 1998; see Figure 15.2.2). In fishes with a branched canal system, canal neuromasts are found only in the canals, not in the highly branched tubules (Blaxter, 1987) and their morphology and distribution are similar to those in narrow-simple canals. In fishes with widened canals, canal neuromasts are located under bony arches at the constrictions located between ballooned out canal segments. These neuromasts are extremely large (up to 1 mm in diameter, personal observation), are shaped like a diamond or cross, and generally

traverse the width of the canal (Garman, 1899; Marshall, 1996; Figure 15.2.2).

The determination of the location of superficial neuromasts in the epithelium of larval or adult fishes requires microscopic analysis using either vital stains (e.g. Blaxter et al., 1983; Tekye, 1990; Mukai and Kobayashi, 1992), histological analysis, or scanning electron microscopy (Tarby, 1998). Alternatively, the location of superficial neuromasts can be determined indirectly by staining the nerves that innervate them (Blaxter et al., 1983; Tekye, 1990). Superficial neuromasts are generally small, and have a round or diamond-shaped outline (Figure 15.2.2). They may occur singly, sitting flush with the epithelium, in small pits, on top of papillae, or on the edge of thin flaps or elongated ridges of skin (Marshall, 1986, 1996; Coombs et

al., 1988). Linear series of superficial neuromasts ('pit lines') have been defined on the head of many fishes (Coombs et al. , 1988; Northcutt, 1989; Webb and Northcutt, 1997). In some teleosts, the pattern of distribution of superficial neuromasts is extremely complex (Tekye, 1990; Wongrat and Miller, 1991) and their innervation and distribution have been used as the basis for phylogenetic reconstruction (Gill and Bradley, 1992). In most fishes, however, superficial neuromast distributions have not been thoroughly assessed.

Morphology of lateral line canals on the trunk In bony fishes, the lateral line canal on the trunk ('the lateral line', or more appropriately, the 'trunk canal') is composed of a series of short canal segments, contained in a linear series of overlapping tubed scales, the lateral line scales. Typical lateral line scales appear as a flat plate with a tube superimposed on it (Figure 15.2.3), but lateral line scale morphology varies tre- mendously among bony fishes (Coombs et al. , 1988; Webb, 1990a; Wonsettler and Webb, 1997). Lateral line scales are covered by a thin layer of epithelium and sit in the dermis beneath the basal lamina as do all fish scales. A pore is present at each end of the canal segment in a lateral line scale (suprascalar and infra- scalar pores; Coombs et al. , 1988; Webb, 1989c). These pores link the canal segments of adjacent overlapping scales which form a continuous epithelium-

lined, fluid-filled canal. Additional pores may pierce the wall of the canal segment and provide additional access to the external fluid environment (Webb, 1990a). A neuromast is generally located in the canal segment (or tube) in each lateral line scale in the trunk canals of bony fishes (Suckling, 1967; Webb, 1989b,c; but see Wonsettler and Webb, 1997).

The placement, number, contour and length of the canal on the trunk varies among bony fishes; eight trunk canal patterns have been described among teleost fishes (Figure 15.2.4; Webb, 1989a). i11 H e t e r o c h r o n y has been suggested as a developmen- m z tal/evolutionary mechanism to explain the evolution of these patterns (Webb, 1989a, 1990b), but functional or adaptive explanations for this variation are lacking, i11

In addition to the neuromast found inside the -t trunk canal, superficial neuromasts, or'accessory neu- m romasts', may be located in the epithelium in close

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proximity to the trunk canal (Coombs et al., 1988), and may continue onto the caudal fin (Webb, 1989c).

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Z position where a canal would be present in other spe- m cies (Webb, 1990b). A limited number of species have a dorsally or ventrally placed canal; other species ( ~ 1 ~ ] have a disjunct canal (Webb, 1990b). In some species, the 'main' trunk canal has one or more branches, which may be represented by a linear series of superficial neuromasts (Northcutt, 1989). In other taxa, mul- O tiple parallel trunk canals lie along the length of the "n trunk (Webb, 1989b). In fishes with multiple trunk z c

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Neuroanatomy of the mechanosensory lateral line system The hair cells that compose the canal and superficial neuromasts are innervated by neurons that

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Figure 15.2.3 Scanning electron micrograph of the trunk canal in the cichlid, Archocentrus nigrofasciatus (= Cichlasoma nigrofasciatum, Webb, 1989a). (A) Two lateral line scales before canal development, showing presumptive canal neuromasts (pcn). (B) Two lateral line scales after canal development showing additional superficial neuromasts (sn) and the suprascalar pore (SSP), which links the canal segment in adjacent scales. (C) Close-up of a presumptive canal neuromast from (A); arrow indicates axis of best physiological sensitivity as determined by hair cell orientation. (D) Anterior end of the trunk canal (just caudal to operculum, op) showing overlapping tubed lateral line scales (from Webb, 1989a, reprinted by permission of Springer-Verlag).

compose a well-defined series of lateral line nerves (Northcutt, 1989; Puzdrowski, 1989; Song and Northcutt, 1991a,b; Figure 15.2.5). These cranial sensory nerves may travel out of the neurocranium with other cranial nerves, but have a series of distinct gang- lia, innervate only neuromasts (and electroreceptors in electroreceptive fishes; Northcutt, 1989) and have well-defined central projection sites in the hindbrain. In fishes, several nerves innervate neuromasts on the head. The anterodorsal and anteroventral nerves (considered by some to be branches of the anterior lateral line nerve, ALLN) innervate the neuromast above and below the eye, and the neuromasts on the cheek, opercular series and mandible (including the preopercular and mandibular canals). The middle lateral line nerve (MLLN) innervates neuromasts in the caudal region of the skull. The posterior lateral line nerve (PLLN) innervates another set of neuromasts in the caudal region of the skull and also innervates the neuromasts on the trunk (Northcutt, 1989).

All of the lateral line nerves project to an octavolateralis column in the hindbrain that consists of the medial octavolateralis nucleus (MON), the caudal octavolateralis nucleus, and the magnocellular nucleus, which are distinguished based on cell morphology and the degree of descending input from higher brain centers that is present. Primary projections of the lateral line nerves are also found in the eminentia granularis of the cerebellum. The MON receives the majority of lateral line input to the central nervous system; the magnocellular nucleus also receives input from the inner ear via nerve VIII (McCormick, 1989, 1997; Puzdrowski, 1989; Song and Northcutt, 1991b; Schellart et al., 1992; New and Singh, 1994; New et al., 1996). Central projections from the mechanosensory lateral line system are generally distinct from those of the auditory system (Finger and Tong, 1984; McCormick, 1989) and the electrosensory lateral line system (New and Singh, 1994). Projection sites of the various lateral line nerves

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Figure 15.2.4 Eight trunk canal patterns found among teleost fishes (from Webb, 1989b, reprinted by permission of Karger).

have been shown to be segregated and demonstrate somatotopy in some species (deRosa and Fine, 1988; Puzdrowski, 1989; Puzdrowski and Leonard, 1993; New and Singh, 1994). The degree to which the projections of different branches of each of these nerves, or inputs from canal versus superficial neuromasts are segregated, is not known. Patterns of central projections vary somewhat among taxa (McCormick, 1982, 1989; Song and Northcutt, 1991b) and there are some differences in projection patterns in fishes that have specialized (McCormick, 1997) and nonspecialized (Schellart et al. , 1992) mechanosensory lateral line systems.

Both canal and superficial neuromasts receive efferent input from the rostral and caudal octavolateralis efferent nucleus in the medulla oblongata, as well as from a diencephalic octavolateralis nucleus (Puzdrowski, 1989; Roberts and Meredith, 1989; Song and Northcutt, 1991b; Schellart et al., 1992; New and Singh, 1994; Wagner and Schwartz, 1996). The efferent system develops early and is already apparent in the larvae of zebrafish (Metcalfe et al. ,

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Functions of the mechanosensory lateral line system The mechanosensory lateral line system allows fishes to respond to unidirectional (d.c.) or oscillatory water movement (a.c., up to 200Hz) at relatively short distances (M/~nz, 1989; Coombs et al. , 1998). Effective lateral line stimuli may arise from prey

Figure 15.2.5 Lateral line nerves and their central projection in bony fishes. (a) Anterior (ALLN), middle (MLLN) and posterior (PLLN) lateral line nerves (in black) with relationship to the other cranial nerves in the Florida ~r gar, Lepisosteus osseus (from Song and Northcutt, 1991a, reprinted by permission of Karger). (b) Lateral view of the central projection areas of the lateral line system in the bowfin, Amia colva. The anterior (ALLN) and posterior ~1 (PLLN) lateral line nerves project to the medial (MON) and cm caudal (CON) octavolateralis nuclei (hatched areas), and -I-1 the magnocellular nucleus (MCN, black) (from McCormick, C Z 1989, reprinted by permission of Springer-Verlag). (c) Cross-sectional diagrams of the primary projections of the --I O anterior (ALLN) and posterior (PLLN) lateral line nerves at Z caudal (left) and more rostral (right) levels in the bowfin, r- Amia calva (from McCormick, 1989, reprinted by permission of Springer-Verlag). z

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(Montgomery, 1989; Bleckmann, 1991; Janssen, 1997; Mohr and Bleckmann, 1998; Montgomery and Coombs, 1998), predators (Blaxter and Fuiman, 1990), neighbors in a school (Bleckmann, 1993; Montgomery et al., 1995), or may be generated by water flow over environmental obstacles (Hassan, 1989). Most recently, it has been shown that the lateral line system transduces vibratory reproductive signals in salmon (Satou et al., 1994) and facilitates rheotaxis (Montgomery et al., 1997). In addition, efferent input (Tricas and Highstein, 1991) and other inputs (Zottoli and Danielson, 1989; Alborg et al., 1996) contribute to, or modify lateral-line-mediated behavior.

The hydrodynamics of fluid movement in response to a vibrating sphere has been used to study the way in which water in a lateral line canal moves in response to a defined external stimulus (Denton and Gray, 1988, 1989; Bleckmann and M/~nz, 1990; Coombs, 1994; van Netten and van Maarseveen, 1994; Montgomery and Coombs, 1998). Such studies have shown that the mechanosensory lateral line system responds to noncompressible, local flow in the near field. Canal and superficial neuromasts respond to the acceleration and the velocity components of the stimulus, respectively (Kalmijn, 1989), and differ in their frequency response properties (M/inz, 1989).

Several model species have emerged in the study of the functional morphology and physiology of the lateral line system. The morphology, development, and physiology of the lateral line system and lateral-line- mediated behavior have been studied extensively in clupeoid fishes (herring and relatives; Blaxter et al., 1983; Denton and Gray, 1983,1993). The mottled scul- pin (Cottus bairdi) has been used extensively to study lateral-line-mediated feeding behavior and the neuro- physiological responses of canal neuromasts to defined hydrodynamic stimuli (Coombs and Janssen, 1990). The ruffe (Acerina, a percid fish), has been used extensively for the experimental analysis of cupular micromechanics and hydrodynamics of fluid movement within its widened head canals (Gray and Best, 1989; van Netten and Khana, 1994). Van Netten and van Maarseveen (1994) have demonstrated that the displacement of the skin overlying the widened canals that occurs in response to a mechanical stimulus accu- rately predicts the movement of neuromast cupulae and thus predicts the response properties of canal neuromasts. In addition, the functional morphology and neurophysiology of the lateral line have been investi- gated in fishes with specialized lateral line morpholo- gies including fishes with multiple trunk canals (Bleckmann and M/inz, 1990; Wonsettler and Webb,

1997) and surface-feeding fishes (Vogel and Bleckmann, 1997; Mohr and Bleckmann, 1998).

Comparative studies have just begun to provide insights into the adaptive functional evolution of the lateral line system. Recent theoretical and empirical work has shown that there are distinct differences in the functional attributes of narrow and widened head canal systems (Denton and Gray, 1988, 1989). Increased canal width, the presence of a flexible instead of a stiff canal roof, and increased size of neuromasts (typical of widened canals) all contribute to increased neuromast sensitivity, but increased response time of widened canal systems (Coombs et al., 1992). In addition, the response properties of extremely wide canals are similar to that of superficial neuromasts (Coombs et al., 1992)..This could account for the evolution of both widened canals and reduced canals (where superficial neuromasts predominate) in deep sea taxa. The ecological significance of functional differences between narrow and widened lateral line systems has been demonstrated recently in two species of percid fishes that use their lateral line systems for prey detection (Janssen, 1997). Interestingly, the nature of structure-function rela- tionships in the lateral line system has been challenged by studies of Antarctic notothenioid fishes in which the frequency response properties of canal neuromasts are not correlated with variation in lateral line canal morphology (Coombs and Montgomery, 1994a,b; Montgomery et al., 1994).

Acknowledgments I thank Drs Sheryl Coombs and John New for helpful discussions. Melissa Tarby granted permission for the reproduction of several original figures. Supported by NSF grant IBN 9603896.

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