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The localization and analysis of the responses to vibration from the isolated elasmobranch labyrinth. A contribution to the problem of the evolution of hearing in vertebrates

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... Around the pores lies the parietal fossa, a parabolic indentation in the dorsal midline of the cranium. The parietal fossa is covered by taut skin, is filled with loose connective tissue (Tester et al. 1972), and is directly connected to the posterior vertical canal of the inner ear via the fenestra ovalis, the largest membranous opening from the otic capsule (Lowenstein and Roberts 1951;Tester et al. 1972;Corwin 1977;Popper and Fay 1977). The posterior vertical canal sometimes hosts an additional sensory epithelium, the macula neglecta (MN) that is found in at least some species of cartilaginous fishes (one patch of MN epithelial tissue in holocephalans, skates and rays, and two patches in sharks) (Retzius 1881;Lowenstein and Roberts 1951;Tester et al. 1972;Corwin 1977;Popper and Fay 1977;Barber et al. 1985). ...
... The parietal fossa is covered by taut skin, is filled with loose connective tissue (Tester et al. 1972), and is directly connected to the posterior vertical canal of the inner ear via the fenestra ovalis, the largest membranous opening from the otic capsule (Lowenstein and Roberts 1951;Tester et al. 1972;Corwin 1977;Popper and Fay 1977). The posterior vertical canal sometimes hosts an additional sensory epithelium, the macula neglecta (MN) that is found in at least some species of cartilaginous fishes (one patch of MN epithelial tissue in holocephalans, skates and rays, and two patches in sharks) (Retzius 1881;Lowenstein and Roberts 1951;Tester et al. 1972;Corwin 1977;Popper and Fay 1977;Barber et al. 1985). In holocephalans, the MN is located near the top of the saccule, behind the utricle, below the sinus superior, and adjacent to the posterior ampulla (Maisey 2001). ...
... In holocephalans, the MN is located near the top of the saccule, behind the utricle, below the sinus superior, and adjacent to the posterior ampulla (Maisey 2001). The epithelium of the MN lacks otoconia, but is covered by a light gelatinous cupula, similar to the cupula covering the neuromasts of the lateral line system (Lowenstein and Roberts 1951;Tester et al. 1972;Corwin 1977). The morphology of the MN shows more inter-specific variation in cartilaginous fishes, notably in size (Corwin 1978), where benthic Proposed auditory pathways in cartilaginous fishes: a the 'otolithic' pathway, where the sound particle motion travels through the fish's body until it reaches the otoconia on the sensory maculae, resulting in the bending of sensory hair cells, and b the 'non-otolithic' pathway, where the sound particle motion travels through the dorsal surface of the head, through the parietal fossa and the fenestra ovalis, until it reaches the macula neglecta, resulting in the bending of sensory hair cells. ...
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Cartilaginous fishes (Chondrichthyes), including sharks, skates, rays, elephant fishes and chimaeras, have been in existence for over 400 million years and represent early stages of the evolution of extant jawed vertebrates. The sensory systems of cartilaginous fishes, including their hearing apparatus, have adapted to a diverse range of ecosystems, from the deep ocean to freshwater rivers, revealing high levels of morphological diversity. Since sound travels such long distances underwater, this environmental cue may represent an important signal in the behavior and survival of this group of fishes but there are still many gaps in our understanding of their hearing system. Based on current knowledge, cartilaginous fishes are most sensitive to low frequency sounds (< 1500 Hz) and there is abundant support that their inner ears use only particle displacement detection rather than the detection of sound pressure, but further studies are needed to corroborate the observations of long distance detection of sound sources that might be based on the detection of pressure oscillations. This review investigates the diversity and functional significance of the inner ear of chondrichthyans from a range of habitats and explores what is known about their hearing capabilities. How underwater sounds are processed by the central nervous system, the impacts of sound on acoustic ecology and behavior , and the potential effects of anthropogenic sound are also examined. Some suggestions for future work are presented to fill the large gaps in our knowledge of the hearing abilities of this important group of vertebrates.
... Due to the properties of water, hearing is only possible for fishes in the range up to ca. 1000 Hz, as the frequencies above this are transmitted poorly or not at all (Maisey 2001;Parmetier et al. 2019). The thousands of sensory hair cells located in the lower part of the inner ear form the sensory macula (Lowenstein and Roberts 1951;Maisey 2001). Within this macula there are granules known as otoliths. ...
... For example, an occlusion of the duct leads to the fact that they (can) lose orientation and balance (Portmann 1921). The vestibular organ is capable of perceiving acceleration, which gives the sharks particular agility and precision during hunting (Lowenstein and Roberts 1951). Young (1981) described in his work that fishes exposed to slower turning speeds have larger semicircular canals than fast swimming fishes. ...
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Elasmobranchs, comprising sharks, skates, and rays, have a long evolutionary history extending back into the Palaeozoic. They are characterized by various unique traits including a predominantly cartilaginous skeleton, superficial prismatic phosphatic layer, and permanent tooth replacement. Moreover, they exhibit a more or less marked sexual dimorphism. Especially the morphology of the chondrocranium and the elements of the whole cranial region of extant and extinct chondrichthyans can provide valuable information about corresponding functions, e.g. the feeding apparatus might reflect the diet of the animals. However, studies on sexual dimorphisms are lacking in orectolobiform sharks, therefore, little is known about possible sexual dimorphic characters in the cra-nial region in this group. For this reason, we present in this study a comprehensive morphological description of the cranial region of the brownbanded bamboo shark Chiloscyllium punctatum Müller & Henle, 1838, with a special focus on its sexual dimorphic characters. Our results reveal clear morphological differences in both sexes of the examined C. punctatum specimens, particularly in the chondrocranium and the mandibular arch. The female specimen shows a comparatively more robust and compact morphology of the chondrocranium. This pattern is also evident in the mandibular arch, especially in the palatoquadrate. The present study is the first to describe the morphology of an orectolobiform shark species in detail using both manual dissection and micro-CT data. The resulting data furthermore provide a starting point for pending studies and are intended to be a first step in a series of comparative studies on the morphology of the cranial region of orectolobiform sharks, including the determination of possible sexual dimorphic characteristics.
... It appears that the sensitivity of the elasmobranch labyrinth to gravitational stimuli is also mediated by the saccular, utricular, and lagenal otolithic organs in addition to the three semicircular canals (Lowenstein and Roberts, 1949). Another mechanotransduction mechanism has also been proposed involving the macula neglecta (Lowenstein and Roberts, 1951;Corwin, 1981). This mechanism relies on the conduction of particle motion into the posterior canal duct through a membrane-covered, fluid-filled opening (the fenestra ovalis) located at the base of a depression (the parietal fossa) in the dorsal chondrocranium (Daniel, 1934;Lowenstein and Roberts, 1951). ...
... Another mechanotransduction mechanism has also been proposed involving the macula neglecta (Lowenstein and Roberts, 1951;Corwin, 1981). This mechanism relies on the conduction of particle motion into the posterior canal duct through a membrane-covered, fluid-filled opening (the fenestra ovalis) located at the base of a depression (the parietal fossa) in the dorsal chondrocranium (Daniel, 1934;Lowenstein and Roberts, 1951). Sound waves, particularly those coming from above and in front, would be transmitted to the endolymph within the posterior dorsal canal and cause local displacements of the cupula of the macula neglecta Corwin, 1977). ...
Chapter
1. Introduction2. The Visual System 2.1. The Eye and Image Formation2.2. Photoreception and Spectral Sensitivity2.3. The Retina and the Choroidal Tapetum2.4. Visual Sampling2.5. Visual Abilities3. The Non-visual System4. The Auditory and Vestibular Systems 4.1. The Inner Ear4.2. Vestibular Control4.3. Auditory Abilities5. The Electrosensory System 5.1. Structure and Spatial Sampling of the Ampullary Organs5.2. Role in Passive Electroreception5.3. Role in Magnetoreception6. The Lateral Line System 6.1. Canal and Superficial Neuromasts6.2. Sensitivity to Hydrodynamic Stimuli7. Cutaneous Mechanoreception8. The Chemosensory Systems 8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances8.2. Olfactory Sensitivity8.3. The Gustatory Apparatus8.4. Gustatory Sampling and Sensitivity8.5. The Common Chemical Sense9. Sensory Input to the Central Nervous System in Elasmobranchs 9.1. Neuroanatomy9.2. Assessing the Relative Importance of Each Sensory Modality9.3. Encephalization9.4. Neuroecology10. Perspectives on Future DirectionsElasmobranchs occupy a diversity of ecological niches with each species adapted to a complex set of environmental conditions. These conditions can be defined as a web of environmental signals, which are detected by a battery of senses, that have enabled these apex predators to survive relatively unchanged for over 400 million years. Signals such as light, odors, electric and magnetic fields, sound, and hydrodynamic disturbances all form a sensoryscape that each species can detect and process. However, the biophysical signals and their propagation within each ecological niche differ and place selection pressures on the ability of a specific sensory modality to detect and respond to prey, predator, and mate. This review investigates how elasmobranchs sense their environment by examining a diversity of species from different habitats, the ways in which they sample their sensoryscape, the sensitivity of each of their senses, and the effect this has on their behavior. The relative importance of each sensory modality is also investigated and how sensory input to the central nervous system can be assessed and used as a predictor of behavior. Although there is still a great deal we do not understand about elasmobranch sensory systems, the anatomical, physiological, molecular, and bioimaging approaches currently being used are enabling us to ask complex behavioral questions of these impressive predators.
... The morphology and functional anatomy of the inner ear of elasmobranchs have already been described in different species (Löwenstein and Sand, 1940;Lowenstein and Roberts, 1951;Tester et al., 1972;Barber and Emerson, 1980;Corwin, 1981a;Maisey, 2001;Lovell et al., 2007). Each inner ear can be divided into two parts forming a membranous labyrinth. ...
... In addition, elasmobranchs possess a fourth canal (the endolymphatic duct) that connects the membranous labyrinth of the inner ear to the external environment (Tester et al., 1972;Mills et al., 2011). The lower part of the inner ear is made up of three chambers (i.e. the saccule, lagena, utricle) that contain thousands of sensory hair cells forming the sensory macula (Lowenstein and Roberts, 1951;Corwin, 1981a;Maisey, 2001). These maculae are overlain by calcium carbonate granules or otoconia (Tester et al., 1972;Corwin, 1989) that act as an inertial mass to stimulate the hair cells (Tester et al., 1972;Hueter et al., 2004). ...
Article
The few works on audition in sharks and rays concern only adult specimens. We report the hearing abilities in the dogfish Scyliorhinus canicula at different stages, from embryos that still have their yolk sac inside their egg, to juveniles. Hearing development corresponds to an increase in the frequency range from 100−300 Hz in early pre‐hatching stages to 100–600 Hz in juveniles. Modifications in hearing abilities correspond to the development of the brain, the increase of the volume of the membranous labyrinth, the growth of the sensory epithelium, and the development of stereocilia in addition to kinocilium before hatching. This work offers solid insights into the development of hearing abilities that usually can only be inferred from the anatomy of vertebrates or after birth/hatching. It shows also that shark can be sensitive to background noise during development.
... The CM has been used extensively in auditory research to study auditory physiology and pathology, increasing our understanding of the cochlear amplifier (Legan et al., 2000;Cheatham et al., 2004), endolymphatic hydrops (Kumagami et al., 1981;Brown et al., 2009), the auditory efferent system (Guinan, 1996), hearing loss due to ototoxicity (Lodhi et al., 1980;Fitzgerald et al., 1993), acoustic trauma (Patuzzi et al., 1989a,b), genetic disorders (Steel et al., 1987) and aging (Harris and Dallos, 1984;Conlee et al., 1988). Conversely, the VM has only featured in a handful of publications mostly involving nonmammalian and ex vivo models (Adrian et al., 1938;Zotterman, 1943;Lowenstein and Roberts., 1951;Corey and Hudspeth, 1983). Trincker (1959) was the first to report in vivo mammalian recordings of the VM, detailing the effects of recording location, stimulus frequency, surgical destruction, cooling and death. ...
... Like the CM, the VM is produced by vibration induced modulation of hair cell conductance, with the extracellular potential determined by changes in current flow through the impedance path between tissue and fluids (Corey and Hudspeth., 1983). However, whilst the CM is dominated by the hair cells local to the recording location (Patuzzi et al., 1989a,b;Cheatham et al., 2011), which are modulated in-phase for low-frequency (<1 kHz) tones, and thus can be used as a reliable estimate the MET channel gating (Patuzzi and Moleirinho, 1998), it is unclear if the same is true for in vivo VM recordings. That is, it is unclear whether the VM is dominated by hair cells local to the recording site, and is therefore dependent upon the orientation of the hair cells (kinocilium) at the sensory epithelium, or is rather the summated extracellular response of all vestibular hair cells (Corey and Hudspeth, 1983). ...
Article
Background: The Vestibular Microphonic (VM) has only featured in a handful of publications, mostly involving non-mammalian and ex vivo models. The VM is the extracellular analogue of the vestibular hair cell receptor current, and offers a tool to monitor vestibular hair cell activity in vivo. Objective: To characterise features of the VM measured in vivo in guinea pigs, using a relatively simple experimental setup. Methods: The VM, evoked by bone-conducted vibration (BCV), was recorded from the basal surface of either the utricular or saccular macula after surgical removal of the cochlea, in 27 guinea pigs. Results: The VM remained after vestibular nerve blockade, but was abolished following end-organ destruction or death. The VM reversed polarity as the recording electrode tracked across the utricular or saccular macula surface, or through the utricular macula. The VM could be evoked by BCV stimuli of frequencies between 100 Hz and 5 kHz, and was largest to vibrations between 600 Hz and 800 Hz. Experimental manipulations demonstrated a reduction in the VM amplitude with maculae displacement, or rupture of the utricular membrane. Conclusions: Results mirror those obtained in previous ex vivo studies, and further demonstrate that vestibular hair cells are sensitive to vibrations of several kilohertz. Changes in the VM with maculae displacement or rupture suggest utricular hydrops may alter vestibular hair cell sensitivity due to either mechanical or ionic changes.
... Rapidly adapting receptors respond to dynamic alterations of the body position occurring with a constant speed in any of the three planes. According to these authors, not only the utricular but also the saccular and lagenar otolith apparatuses are involved in the control of the static equilibrium (Schoen and Holst, 1950;Löwenstein and Roberts, 1951). These data were more recently supported experimentally Schellart and Popper, 1992). ...
Article
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This paper describes basic information about the labyrinth and equilibrium sense in fish. The anatomy and morphology of semicircular canals and otolith organs are considered. It also describes structural characteristics of otoliths of different types (central, amorphous, composite, and polycrystallic); their morphologic diversity; the structure of the otolith membrane, orientation of receptor cells in the maculas of semicircular canals, utriculus, sacculus, lagena and in macula neglecta; innervation of these sensory structures; and the principle of their functioning as detectors of lateral (semicircular canals) and linear (otolith organs) accelerations. The relationship between the functional parameters of the otolith apparatus (absolute and differential sensitivity, performance, and the range of acceleration perceived) and the mass of the otolith is analyzed. The differences in the size of the lapillus, sagittae, and asteriscus; the retention of these differences throughout the life of the individual; and the continuous growth of otoliths are noted, along with the significance of the simultaneous presence of otoliths with different masses in fish with different life modes. Information about the vestibular function in fish with an unusual spatial orientation of the body is presented. The participation of visual and tactile systems in the maintenance of equilibrium and in the dorsal light reflex (Lichtrückenreflex) and the vestibular–ocular reflex are analyzed. The significance of the equilibrium sense in different behavioral patterns—migration and swimming, including those under insufficient illumination—are analyzed. The time course of the ontogeny of basic labyrinth structures is traced, as well as the features of the appearance and development of the sense of equilibrium in fish. It is noted that the functioning of many aspects of the vestibular system has been insufficiently studied.
... As well, chondrichthyans have an additional maculae (area of neuromast-based sensory epithelium) called the macula neglecta (MN) (Fig 6C red). It is not covered by octonial mass but is associated with the posterior semicircular canal (green) and is important for sound detection at least in elasmobranchs (Lowenstein and Roberts 1951;Fay et al. 1974;Corwin 1989). Free swimming, piscivorous elasmobranchs tend to have a larger sacculus and posterior semicircular canal duct and a more complex, larger macula neglecta than bottomdwelling, non-piscivorous species which suggests that the former have better hearing than the latter (Myrberg 2001). ...
Chapter
Chondrichthyans are one of two major clades of living jawed vertebrates, with a rich fossil record potentially extending back to the Late Ordovician (455 million years ago, mya). The main groups of chondrichthyans include the chimaeroids, sharks, and skates and rays. This chapter outlines the major events in chondrichthyan evolution, focusing on features of the cranium, jaw and jaw musculature, and gill arch skeleton. The “spiny sharks” (acanthodians) and other stem chondrichthyans have recently been shown to exhibit a mosaic of chondrichthyan and osteichthyan characters. Taxa such as iniopterygians and chondrenchelyiforms, resolved as stem group chimaeroids, appear in the Carboniferous and display dramatic body forms and unusual fin morphology. Chondrichthyans also show a considerable range of dentitions, both in terms of morphology and development, particularly modified in the chimaeroids. In addition to their differing tooth morphologies, chondrichthyans have several types of jaw suspensions to support a range of feeding and breathing modes. Sharks have well-developed brains that vary according to the environment rather than phylogeny. Their senses are also well-developed and finely tuned to best perform in their particular ecological niche. The long evolutionary history of chondrichthyans and their great diversity as well as the retention of some primitive characters make them good models for evolutionary and developmental studies.
... All the sharks tested show mainly low-frequency sensitivity, and there is no evidence that they are more sensitive at low frequencies than other fishes (Kritzler and Wood, 1961; Banner, 1967; Nelson, 1967; Kelly and Nelson, 1975; Casper et al., in press). Several papers show the importance of the macula neglecta in detecting sound and/or vibration (Lowenstein and Roberts, 1951). Fay et al. (1974) measured the response of the macula neglecta to vibrational stimuli applied to the parietal fossa. ...
... The vertebrate auditory system was more refined and had developed special tasks like acoustic feature discrimination, sound source localization, frequency analysis and auditory scene analysis in coordination with the visual inputs. These sorts of capabilities arose very early in the evolution of the vertebrates and have been modified by selection in different species [12,13,16]. Refinements to the ear in Mammals occurred rapidly due to multiple episodic genetic evolution of 'prestin' -the functional motor protein of cochlear outer hair cells providing robust hearing capacity and this may have been the reason for mammals to adapt and dominate over other species [14,15]. ...
Article
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The evolution of the human ear is a fascinating story of the formation and adaptation by trial and error of a primitive sound receptor. Human hearing is thus the end product of long and complex evolutionary steps, its primordium having first evolved from gill slits & jawbone of ancient fishes. Hearing is the most vital special sense organ to form the basis for communication by which civilization of the human race has taken place thus far. Knowing this evolutionary pathway will enable us to reason out the complex anatomy of human hearing in a better way. This review article is a synopsis from a number of scientific contributions in literature, which chronologically trace the origin & adaptations of the hearing apparatus from the era of fishes up to human life. It is paramount that the phylogeny & evolution of human hearing should be understood as it plays an important role in the understanding of the basis of congenital anomalies & inner ear pathophysiology. This knowledge will further help in propagation of evidence based clinical practice while managing various complex ear anomalies which we encounter in the present day.
... The VM was first reported just 8 years after the CM in 1938, albeit in an ex vivo preparation (Adrian et al., 1938;Zotterman, 1943;Lowenstein and Roberts, 1951;Wever and Vernon, 1956). Since then, the VM has been recorded in vivo in zebrafish (Trapani and Nicolson, 2010;Yao et al., 2016), toadfish (Rabbitt et al., 1995), bullfrogs (Eatock et al., 1987), pigeons (De Vries and Vrolijk, 1953;Wit et al., 1986Wit et al., , 1990, and guinea pigs (Trincker and Partsch, 1959). ...
Article
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Electrocochleography (EcochG), incorporating the Cochlear Microphonic (CM), the Summating Potential (SP), and the cochlear Compound Action Potential (CAP), has been used to study cochlear function in humans and experimental animals since the 1930s, providing a simple objective tool to assess both hair cell (HC) and nerve sensitivity. The vestibular equivalent of ECochG, termed here Electrovestibulography (EVestG), incorporates responses of the vestibular HCs and nerve. Few research groups have utilized EVestG to study vestibular function. Arguably, this is because stimulating the cochlea in isolation with sound is a trivial matter, whereas stimulating the vestibular system in isolation requires significantly more technical effort. That is, the vestibular system is sensitive to both high-level sound and bone-conducted vibrations, but so is the cochlea, and gross electrical responses of the inner ear to such stimuli can be difficult to interpret. Fortunately, several simple techniques can be employed to isolate vestibular electrical responses. Here, we review the literature underpinning gross vestibular nerve and HC responses, and we discuss the nomenclature used in this field. We also discuss techniques for recording EVestG in experimental animals and humans and highlight how EVestG is furthering our understanding of the vestibular system.
... The macula neglecta consists of one or two patches of sensory hair cells that show a variety of orientations. The variation in the structure of the macula neglecta has been hypothesized to be linked to the foraging behavior (Corwin 1978), and several studies have shown the importance of the macula in detecting sound and/or vibration (Lowenstein and Roberts 1951). Despite the auditory system being better described in elasmobranchs, some differences have been reported for chimaeras' auditory system. ...
Chapter
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Chondrichthyes’ sensory systems are part of the nervous system responsible for receiving external and internal stimuli and translating them into nerve impulses that are transmitted to the central nervous system where they are processed.
... All Rights Reserved origin, and since they are anatomically located next to each other, the proximity of the saccule to the stapes may explain its mechanical stimulation during sound stimulation [1]. Moreover, in lower species the saccule functions as an acoustic receptor and in some vertebrates it serves as the only acoustic organ [6], [7]. Furthering this idea of an integrated auditory-vestibular system is the fact that the two systems share common target projections within the cortical temporo-parietal areas [8]. ...
Article
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Sound is known to affect the human brain, hence sound or music therapy is sometimes used to improve a subject's physicaland mental health. In this study, the effects sound stimulation has on balance were investigated by means of computerizeddynamic posturography tests performed with eyes closed on an unstable surface using a CAPS® system, exceeding theInternational Society for Posture and Gait Research (ISPGR) recommended metrological performance standards. Subjectswere tested without listening to any music (baseline), listening to “pure music”, and listening to the same music with differenttones embedded into it (one for each key). We found that different subjects react differently to different tones. Music alonedid not have a statistically significant effect on balance compared to the baseline, but the “best” tone significantly improvedbalance compared to the baseline or the “pure music” conditions. Furthermore, the “worst” tone reduced the balancecompared to “pure music”, but the reduction was not statistically significant relative to the baseline. The results thereforeindicate that, at least relative to balance performance, the tone-based sound stimulation we investigated is effective andinherently safe, but that tone selection depends on the individual subject.
... The hearing range of elasmobranchs studied to date falls within the range of 20-1000 Hz with greatest sensitivities at lower frequencies [3,[9][10][11][12]. Elasmobranch and teleost ears are both comprised of inner ear labyrinths containing a saccule, lagena, utricle, otoliths and three semicircular canals; however, the elasmobranch ear is unique in that it also contains the macula neglecta, which, combined with the sacculus, is thought to be used for hearing [13][14][15]. Elasmobranchs detect sound through particle motion (not pressure) because they lack a swim bladder and specialized hearing structures [4,9,[16][17][18][19] which typically act as pressure-to-displacement transducer organs in teleosts. ...
Article
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The ability of elasmobranchs to detect and use sound cues has been heavily debated in previous research and has only recently received revived attention. To properly understand the importance of sound to elasmobranchs, assessing their responses to acoustic stimuli in a field setting is vital. Here, we establish a behavioural audiogram of free-swimming male and female southern stingrays (Hypanus americanus) exposed to low-frequency tones. We demonstrate that female stingrays exposed to tones (50-500 Hz) exhibit significant changes in swimming behaviours (increased time spent swimming, decreased rest time, increased surface breaches and increased side swimming with pectoral flapping) at 140 dB re 1 µPa (-2.08 to -2.40 dB re 1 m s-2) while males exposed to the same tones did not exhibit a change in these behaviours until 160 dB re 1 µPa (-1.13 to -1.21 dB re 1 m s-2). Our results are the first demonstration of field responses to sound in the Batoidea and show a distinct sensitivity to low-frequency acoustic inputs.
... In lower vertebrates, such as elasmobranchii (i.e. skates, rays and sharks; Lowenstein and Roberts, 1951), frogs (Ashcroft and Hallpike, 1934a,b;Christensen-Dalsgaard and Narins, 1993;Koyama et al., 1982), toads (Moffat and Capranica, 1976) and fish (Popper and Fay, 1973), the otoliths are extremely sensitive to vibration. For example, saccular fibres of the frog Leptodactylus albilabris have a threshold to vibration as low as 0.001 cm/s 2 (10 -6 g), within a preferred frequency range of approximately 20-300 Hz (Narins and Lewis, 1984). ...
... While cochlear microphonic has extensively been used to examine hair cell and cochlear function, vestibular microphonic has only been reported in a handful of publications mostly involving non-mammalian and ex vivo models (Adrian et al., 1938;Zotterman, 1943;Lowenstein and Roberts, 1951;Corey and Hudspeth, 1983;Rabbitt et al., 2005). Trincker (1959) used air-conducted sound to stimulate the vestibular system, and maintained fluid within the vestibule following surgical destruction of the cochlea, whereas Pastras et al. (2017) measured vestibular microphonic from utricular or saccular macula using bone-conducted vibration. ...
Article
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The mammalian inner ear has two major parts, the cochlea is responsible for hearing and the vestibular organ is responsible for balance. The cochlea and vestibular organs are connected by a series of canals in the temporal bone and two distinct extracellular fluids, endolymph and perilymph, fill different compartments of the inner ear. Stereocilia of mechanosensitive hair cells in the cochlea and vestibular end organs are bathed in the endolymph, which contains high K ⁺ ions and possesses a positive potential termed endolymphatic potential (ELP). Compartmentalization of the fluids provides an electrochemical gradient for hair cell mechanotransduction. In this study, we measured ELP from adult and neonatal C57BL/6J mice to determine how ELP varies and develops in the cochlear and vestibular endolymph. We measured ELP and vestibular microphonic response from saccules of neonatal mice to determine when vestibular function is mature. We show that ELP varies considerably in the cochlear and vestibular endolymph of adult mice, ranging from +95 mV in the basal turn to +87 mV in the apical turn of the cochlea, +9 mV in the saccule and utricle, and +3 mV in the semicircular canal. This suggests that ELP is indeed a local potential, despite the fact that endolymph composition is similar. We further show that vestibular ELP reaches adult-like magnitude around post-natal day 6, ~12 days earlier than maturation of cochlear ELP (i.e., endocochlear potential). Maturation of vestibular ELP coincides with the maturation of vestibular microphonic response recorded from the saccular macula, suggesting that maturation of vestibular function occurs much earlier than maturation of hearing in mice.
Chapter
The class Chondrichthyes or cartilaginous fishes comprises about 800 species belonging to two major radiations that have diverged over 350 million years ago, i. e. the elasmobranchs and the holocephalians (Compagno 1977; Carroll 1988). Fossil evidence suggests that living holocephalians are a much older form than modern elasmobranchs, which arose approximately 200 million years ago (Carroll 1988). The living elasmobranchs (sharks, skates and rays) comprise four major superorders: Squalomorphii, Galeomorphii, Squatinomorphii and Batoidea (Table 12.1). The elasmobranchs are widely distributed, as they are marine in habitat, except for one species, Carcharinus leucas, which lives in Lake Nicaragua and in estuaries of large rivers, such as the Ganges, the Mississippi and the Zambesi. There are about 350 described living species of sharks, ranging in size from the giant whale shark (up to 15 m long) and basking shark (up to 10 m long) to tiny ones such as Squaliolus laticaudus, which in adulthood measures 15 cm in length. Paradoxically, the largest sharks mentioned above are plankton feeders and quite harmless. Of the 350 species of living sharks, no more than 35 have been implicated in attacks on humans (Gilbert 1984).
Article
Retzius (1881, 1884) reviewed earlier literature and reported the first extensive studies of the anatomy of the internal ear in lower vertebrates representing diverse taxonomic assemblages. Despite the limitations of techniques then available, the general accuracy, attention to detail, and superb illustrations that characterized those reports have made them classics in the field, and they are still widely cited as sole or primary anatomical source material in aural studies. During the ensuing fifty years, technical advances in light microscopic techniques were applied to circumscribed problems concerning the ear in lower vertebrates, but major interest centered about transmission mechanisms in those animals and on the labyrinth in mammals. A second major reference source appeared at the end of that period when de Burlet (1934) summarized many of the previous studies and added significant new information on the periotic (perilymphatic) labyrinth. Since the appearance of the de Burlet publication, Werner (1960) has offered a broad comparative anatomical coverage of the ear, but the most recent reviews related to submammalian auditory anatomy limit their coverage to specific taxonomic assemblages and/or incorporate anatomical information within a treatment of hearing (van Bergeijk, 1967; Schwartzkopff, 1968; Baird, 1970a; Lowenstein, 1971; Lavolga, 1971; Smith and Takasaka, 1971).
Article
Members of all vertebrate groups have sensory receptors to detect sound energy, though their capabilities are diverse. There are two components to sound, the pressure wave and particle motion, either or both of which may be encoded by the peripheral auditory system. The transition from aquatic to terrestrial life among vertebrates may have been accompanied by an increased dependence on the information conveyed by the pressure component of sound, since the pressure wave is detectable from greater distances than particle motion. Changes in the peripheral auditory system appear to have influenced the organization of the central auditory system, which exhibits similar organization and physiological responses in all vertebrate groups. Frequency tuning, the emergence of binaural comparisons, feature detection, convergence of sensory modalities, and descending modulation have been shown in all groups. Thus, the central auditory systems of modern vertebrates show many examples of parallel solutions to similar problems.
Chapter
The emergence of the vertebrates during organic evolution is still obscure. Zoologists find it impossible to single out any specific invertebrate type as the direct ancestor of one or the other of the earliest fish-like vertebrates. The proto-chordates point the way but there is rather a wide gap between them and the Agnatha or jawless fishes. These include the ostracoderms, the earliest known fossil chordates, and the living cyclostomes, hagfishes and lampreys. In both the ostracoderms and the cyclostomes the labyrinth has reached almost the extent of organization characteristic throughout the vertebrates. Its subdivision into semicircular canals and otolith organs is phylogenetically fundamental and is found in the labyrinth of the fossil ostracoderm Kieraspis (Stensiö, 1927) and in the cyclostomes.
Article
The late nineteenth and early twentieth centuries witnessed rapid growth in descriptive neuroanatomy. This period of intensive study of nervous systems in a wide variety of vertebrates resulted in several hypotheses concerning the origin and subsequent evolution of the otic and lateralis systems. These hypotheses possess two common features: they are based on descriptive anatomical material and were not tested experimentally as the appropriate techniques did not yet exist; and they reflect certain supposed anatomical relationships among an amniotic vertebrates that were believed to form a linear series of increasingly complex groups.
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With the development of methods for histochemical analysis of inner ear structures, tissue culture techniques, phase-contrast microscopy, X-ray diffraction, and electron microscopy, the knowledge of inner ear structures has rapidly progressed. This chapter discusses the structure and peripheral innervation of the inner ear. The inner ear is surrounded by a very hard and, from a histotechnical point of view, resistant bony capsule. This periotic labyrinth is subject to many investigations, especially as the bone is the site of a special disease, otosclerosis–a disease, which today is the object of otologic surgical interest. The chapter describes the development and the general features of the bony labyrinth and the inner ear. In the adult mammalian ear the periotic labyrinth encapsules the otic labyrinth which consists of a series of ducts and sacs floating in or supported in the perilymph by thin, fibrous strands or by nerve fibers. The communication with the surrounding fluid systems takes place through the endolymphatic duct and the cochlear aqueduct. Through the oval and round windows sound waves may enter the inner ear. The chapter also focuses on the structure and innervation of the cochlea and vestibular sensory epithelia.
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The experiments of Goltz (1870), Mach (1873), Breuer (1891), Ewald (1892), Bárány (1907) and Steinhausen (1931, 1933) can be considered as a very important first step in the development of the physiology of the vestibular system. They established a theory of the mechanics of the peripheral vestibular sensory mechanisms which is still basically valid today. The various sensory cells in the peripheral vestibular sensory organ serve as receptors for linear and angular accelerations about different axes, thus providing a three dimensionally organized sensory system for orientation in space. Various other sensory systems such as the visual, somatosensory and acoustic apparatus combine with the vestibular organs in assuring a high sensitivity for the adjustment of the body in space. Part of this regulation is achieved by means of interaction in the vestibular nuclei which integrate the activity of the various vestibular receptors as well as the activity of other sensory structures which converge directly or indirectly on the vestibular neurones. As the vertebrates developed from lower to higher forms other sensory systems such as the somatosensory and visual systems became more and more important in the regulation of posture; however, the vestibular nuclei still remain an important integrative structure that deserves the interest of anatomists as well as physiologists.
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This chapter, written from the perspective of four authors who have been studying fish bioacoustics for over 120 years (cumulative!), examines the major issues of the field. Each topic is put in some historical perspective, but the chapter emphasizes current thinking about acoustic communication, hearing (including bandwidth, sensitivity, detection of signals in noise, discrimination, and sound source localization), the functions of the ear (both auditory and vestibular, and including the role(s) of the otoliths and sensory hair cells) and their relationships to peripheral structures such as the swim bladder, and the interactions between the ear and the lateral line. Hearing in fishes is not only for acoustic communication and detection of sound-emitting predators and prey but can also play a major role in telling fishes about the acoustic scene at distances well beyond the range of vision. The chapter concludes with the personal views of the authors as to the major challenges and questions for future study. There are still many gaps in our knowledge of fish bioacoustics, including questions on ear function and the significance of interspecific differences in otolith size and shape and hair cell orientation, the role of the lateral line vis-à-vis the ear, the mechanisms of central processing of acoustic (and lateral line) signals, the mechanisms of sound source localization and whether fishes can determine source distance as well as direction, the evolution and functional significance of hearing specializations in taxonomically diverse fish species, and the origins of fish (and vertebrate) hearing and hearing organs.
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One of the most striking features in the auditory system of fishes is the extensive structural diversity in the inner ear and its peripheral accessories. In this chapter we will summarize this diversity in the ear, from the gross structure to the ultrastructure of the sensory epithelia, and suggest some of the possible functional meanings for these structural differences. We hope that this discussion will stimulate interest in pursuing direct experimentation on the function of the fish ear in order to fill in the gaps in our understanding of peripheral auditory mechanisms. Two major points will be stressed throughout this chapter. First, we feel that dividing up of auditory and vestibular functions between the different otolithic organs of the ear may not be as absolute as has been often implied, so it may be necessary to reconsider some of the basic “classical” assumptions of auditory organ functions, at least with regard to the teleost ear. Second, we suggest that the notion of a functionally or structurally “typical teleost ear” is no longer tenable, since the breadth of interspecific structural variation in teleost ears may imply significant functional variation.
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During natural movement on the earth’s surface, we are seldom aware of vestibular sensations, and when we do become aware of them, they usually signify an unnatural stimulus or an abnormality of vestibular function. With specially contrived conditions of observation, relationships between acceleratory stimuli and vestibular sensations and perceptions can be described quantitatively and qualitatively. These relationships constitute the primary subject matter of this chapter, but to appreciate this material in relation to daily experiences, we must first consider why vestibular sensations do not typically achieve conscious awareness during natural voluntary head and body movement.
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Elasmobranchs (sharks, skates, and rays) have evolved little over a span of hundreds of millions of years, presenting an opportunity to study one of the most basal stages in the evolution of vertebrate audition. The ears of elasmobranchs, while similar to those found in teleost fishes and even terrestrial vertebrates, are also unique among fishes in that they have an opening from the inner ear to the surface of the head called the endolymphatic duct. The ears in elasmobranchs are also specialized in that the macula neglecta end organ, which is diminutive in all other vertebrates, is large and appears to have a major role in hearing. However, there appear to be numerous morphological differences within the macula neglecta and other auditory structures of benthic and pelagic elasmobranchs that could be attributed to lifestyle and feeding behavior. The relative importance of hearing in the behavior of elasmobranchs compared with other senses is unclear, though many species of sharks have been shown to be attracted to acoustic stimuli from distances as far as hundreds of meters.
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The inner ear and lateral line form the octavolateralis system in aquatic vertebrates. This system provides an array of electrosensory and mechanosensory inputs that are integrated with chemosensory and visual information to produce behavioral responses appropriate for the organism (see Blaxter 1988). As several chapters in this volume note (Enger et al. Chapter 29; Kalmijn Chapter 9), there are structural and functional parallels between the inner ear and the mechanosensory lateral line systems. Direct comparisons between these systems are useful with regard to the phylogeny, ontogeny, micromechanics, transduction processes, coding, central connections, and behavioral use of these organs. Just as research on the lateral line has advanced our understanding of inner ear function (see Flock 1974), insights gained from vestibular and auditory research might help to guide questions regarding lateral line function. This chapter addresses some parallels between the mechanosensory lateral line and the ear of fishes and considers how investigators of these two systems might learn from one another.
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An inner ear containing multiple sensory endorgans arose early in vertebrate history. Among jawed vertebrates the ear includes seven endorgans believed to be primitive for jawed fishes (otolithic endorgans: utricle, saccule, lagena; macula neglecta; three semicircular canals) as well as the various derived papular endorgans of anamniotes (amphibian and basilar papillae) and amniotes (basilar papilla or cochlear duct). What is remarkable about this collection of endorgans is that, with the exception of the semicircular canal cristae, each of the remaining endorgans has been implicated in hearing in one species or another. The classic notion that the otolithic endorgans do not contribute to hearing in land vertebrates has been recently disproven in amphibians (reviewed in Lewis et al. 1985), a discovery that challenges us to reexamine otolithic endorgan function in other vertebrates. Moreover, it has also been recently claimed that the evolution of the papillar endorgans, at least of anamniotes, predates the emergence of vertebrates onto land (Fritzsch 1987, Chapter 18), a view that requires us to reconsider the selective pressures that influenced the appearance of acoustic receptors.
Article
Studies on the auditory system of fishes can provide fundamental information about the early evolution of vertebrate hearing. While there are limited data available on the auditory system of bony fishes, comparatively far less is known about auditory structures in elasmobranchs, despite their critical basal position within vertebrate evolution. Specifically, while there is a high degree of plasticity in the nervous system, little is known about how the different sensory epithelia within the inner ear vary throughout life in elasmobranchs. Using a combination of immunohistochemistry and fluorescence microscopy, we quantified macular area, number of sensory hair cells, hair cell density, and hair cell orientations in the saccule, lagena, utricle, and macula neglecta of school sharks (Galeorhinus galeus) of varying body size. In all maculae, macular area and the number of hair cells increased significantly throughout ontogeny, while hair cell density displayed a concurrent ontogenetic decrease (excluding the utricle). There were also significant differences in macular area, hair cell number, and hair cell density between the four maculae. However, hair cell orientation patterns did not vary between individuals and did not change with body growth. These findings represent one of the first comprehensive characterisations of the inner ear sensory epithelia in an elasmobranch, and reveal changes in morphology that may have implications for auditory capabilities through ontogeny.
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It has been known for many years that the human eyes are never quite motionless, even when steadily fixed at a point target (Adler and Fliegelmann, 1934). One particular component of the incessant motion is a very rapid tremor of the eyes. The amplitude of this tremor movement is usually less than 30 seconds of arc. This means that the amplitude of vibration of a point on the surface of the cornea is of the order of 0.001 mm. The frequency spectrum is concentrated mainly below 100 Hz, but sometimes extends to approximately 150 Hz. The tremor has horizontal (abduction-adduction), vertical (elevation-depression) and torsional components.
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Vestibular research currently relies on single response measures such as ex vivo hair cell and in vivo single unit recordings. Although these methods allow detailed insight into the response properties of individual vestibular hair cells and neurons, they do not provide a holistic understanding of peripheral vestibular functioning and its relationship to vestibular pathology in a living system. For this to take place, in vivo recordings of peripheral vestibular nerve, hair cell and mechanical function are needed. The previous inability to record vestibular hair cell responses stemmed from a difficulty in accessing the vestibular end-organs and stimulating them in isolation of the cochlea. To circumvent this, we developed a ventral surgical approach, removing the cochlea, to provide full access to the basal surface of the utricular macula. This allowed functional and mechanical utricular hair cell recordings, alongside gross utricular nerve responses. Recordings were performed in anaesthetized guinea pigs using Bone Conducted Vibration (BCV) and Air Conducted Sound (ACS) stimuli, providing a clinical link to vestibular reflex testing. We have thus far performed experiments involving: 1) Selective manipulation of vestibular nerve function, using electrical stimulation of the central vestibular system. 2) Glass micropipette recordings from the basal surface of the macular epithelium, which provided a robust and localized measure of extracellular utricular hair cell function. 3) With the macular exposed, we have measured the dynamic motion of the macula using Laser Doppler Vibrometry, which was recorded alongside the hair cell and nerve response recordings. 4) We have used physiological and pharmacological experimental manipulations to selectively modulate utricular nerve, hair cell or mechanical function, demonstrating the ability to differentially diagnose the basis of peripheral vestibular disorders in the mammalian utricle. These tools allow for a more complete understanding of peripheral vestibular function and a first order perspective into clinical disorders effecting the otoliths.
Article
Older studies of mammalian otolith physiology have focused mainly on sustained responses to low-frequency (<50 Hz) or maintained linear acceleration. So the otoliths have been regarded as accelerometers. Thus evidence of otolithic activation and high-precision phase locking to high-frequency sound and vibration appears to be very unusual. However, those results are exactly in accord with a substantial body of knowledge of otolith function in fish and frogs. It is likely that phase locking of otolith afferents to vibration is a general property of all vertebrates. This review examines the literature about the activation and phase locking of single otolithic neurons to air-conducted sound and bone-conducted vibration, in particular the high precision of phase locking shown by mammalian irregular afferents that synapse on striolar type I hair cells by calyx endings. Potassium in the synaptic cleft between the type I hair cell receptor and the calyx afferent ending may be responsible for the tight phase locking of these afferents even at very high discharge rates. Since frogs and fish do not possess full calyx endings, it is unlikely that they show phase locking with such high precision and to such high frequencies as has been found in mammals. The high-frequency responses have been modeled as the otoliths operating in a seismometer mode rather than an accelerometer mode. These high-frequency otolithic responses constitute the neural basis for clinical vestibular-evoked myogenic potential tests of otolith function.
Article
The electrical responses of single hair cells of the ear of fish were recorded by means of an intracellular microelectrode. 1) DC potential between the peri- and the endolymph measured. 5-7mV, the latter being always positive in reference to the former. 2) The resting potential of the hair cells in ampullae was 10- 12mV, while that in the utricule was 8-10mV. 3) Responses of those cells in ampullae to rotatory stimuli were reverse to each other, depending on the direction of rotation.In the horizontal canal the ampullopetal acceleration produced a depolarisation and the deceleration a repolarisation and, if any, , hyperpolarisation, whereas the ampullofugal acceleration produced a hyperpolarisation and the deceleration a depolarisation.In the vertical canals, both anterior and posterior, just the reverse responses were observed.The validity of Ewald's old hypothesis was identified. The ampulla was also responsive to the linear movement. 4) Responses of hair cells of the utricule were substantially not so much different from those of the ampulla. They were very remarkable to the linear movement but the utricule was still responsive to the rotation. 5) All these responses have never shown the overshoot.
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The sense of hearing in fish is anatomically localized to the pars inferior of the labyrinth (comprising sacculus and lagena) while the site of the equilibrium function is in the pars superior (utriculus and ampullae of the semicircular canals) (Fig. 1) (von Frisch and Stetter, 1932; von Frisch, 1936, 1938; Dijkgraaf, 1949). The functional role of the various parts of the labyrinth is not absolutely strict, however, since the lagena seems to have essentially an equilibrium function in elasmobranchs (Lowenstein and Roberts, 1949, 1951) and an auditory function in teleosts. It has also been shown that the utriculus may perceive sound in teleosts (Dijkgraaf, 1949).
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At a previous symposium on hearing in fishes organized by Dr. Tavolga, van Bergeijk (1964) put forward some important ideas about the properties of sound in water and imparted to the lateral line system a significant role in the localization of sound sources, thereby appearing to settle the troubling question of the biological significance of these sense organs.
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The labyrinth represents the final stage in the process of submergence of neuromast organs of the lateral line type, and it has become completely or, at any rate, almost completely, separated from the outside medium and enclosed in the brain case. The ductus endolymphaticus maintains a tenuous connection with the outside world in the elasmobranchs only. The typical subdivision of the laybrinth into semicircular canals and otolith organs is phylogenetically fundamental, and is found in the labyrinth of the cyclostomes and in the fossil ostracoderm Kiaermpis. Two types of otoliths are known. The first is solid and of a constant shape characteristic of the species and in fact of the specific otolith organ within the labyrinth. The solid otoliths are anchored to the membranous wall of the labyrinth by systems of connective tissue strands functioning like guy ropes. Such structures are sparingly developed in connection with paste like otolithic masses. In the latter , the otolithic mass of one otolith organ can be continuous with that of another. In the elasmobranch labyrinth, such continuity has been observed between otolithic masses in sacculus and lagena.
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This chapter on the foundations of vestibular science will focus attention on the historical and technological factors which have operated in the advance of the subject during the past five decennia.
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Otolithic organs have been classically considered as accelerometers with a practically flat gain-frequency curve (26). However, a closer look into the responses recorded from the otolithic afferent nerves reveals a more complex input-output relationship (9,10,22,23). Otolithic organs do not respond to changes in the acceleration vector in a linear way: they are sensitive to high frequency vibrations in a nonlinear fashion (21). Linear accelerations of the same amplitude but opposite sense elicit different responses from otolithic organs (9). Because of adaptation (23), otolithic organs can respond phasically to a sustained mechanical stimulus, and as a result their gain frequency curves have a positive slope. Furthermore, all the afferents innervating a given organ do not respond identically to the same stimulus (23). This complexity makes it difficult to consider the otolithic organs as simple accelerometers, and makes a characterization of the different afferents neeessary.
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This article presents a current assessment of elasmobranch auditory biology and an evaluation of future directions for research. Excellent review articles have recently detailed the pre-1975 development of this field (Popper and Fay 1977, Myrberg 1978), so I will not emphasize that work. Instead, I will focus on more recent investigations, including some new data.
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The inferior division of the inner ear (saccule and lagena) is considered the primary area of audition in most fishes and has received most of the attention in anatomical investigations of the labyrinth. Recent ultrastructural studies have provided information on surface features of the sensory areas in numerous species, defining various polarization patterns and several types of hair cell bundles. Speculation on the function of particular types of hair cells has been possible to some extent based on physiological data available on the inferior division. The ultrastructure of the superior division of the labyrinth has received less attention; this may be due, at least in part, to indications that anatomically this region displays less interspecific diversity than the inferior division, and functionally the superior division is considered primarily a gravistatic organ in most fishes (Lowenstein 1971). Differences in the types of hair cell bundles have been reported in the utricular maculae of a few osteichthyan species (Dale 1976, Platt 1977, Popper 1978). Attempts to interpret the functional significance of these bundles has often been based upon their presence in sensory areas other than the utricular macula, sometimes in different species, where the function of the region is better known. If bundle type indicates specific function, the presence of cells in the utricle that are similar to those in areas of the inner ear not considered as gravistatic organs suggests that the utricular macula in osteichthyans may have more than one function.
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The auditory capacities of fish have recently been reviewed by Tavolga (1971), Popper and Fay (1973), Hawkins (1973) and Fay and Popper (1980), following early reviews by Griffin (1950), Kleerekoper and Chagnon (1954), and Moulton (1963). Not only can fish hear but they can distinguish between tones of differing frequency (Wohlfahrt 1939, Dijkgraaf and Verheijen 1950, Dijkgraaf 1952, Jacobs and Tavolga 1968, Fay 1970). For an ostariophysine fish, the goldfish, Carassius auratus, relative pitch discrimination lies between 3–6% (Jacobs and Tavolga 1968), and for several nonostariophysines it lies between 9 and 15% (Dijgraaf 1952).
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The octavolateralis system collectively comprises four classes of sensory end organs and their neuronal connections. These end organs—the auditory and vestibular receptors of the inner ear and the electroreceptors and mechanoreceptors of the lateral line system—have as their sensory elements hair cells or cells believed to be modified hair cells. Various aspects of the octavolateralis system have been repeatedly reviewed in recent years. Information regarding receptor morphology and central anatomy and physiology can be found in this volume (Chaps. 9, 22, 23, 28 and 31–33), as well as in others (e.g., Fessard 1974; Tavolga, Popper, and Fay 1981; Northcutt and Davis 1983; Bullock and Heiligenberg 1986). In this chapter we shall consider the octavolateralis system with respect to the following question: What is the relationship between major evolutionary changes in the sensory periphery and the organization of the CNS? Comparative anatomical and physiological studies have revealed that the octavolateralis system has a complicated and apparently unusual evolutionary history including the loss, invention, and “reinvention” of various receptor classes. It is thus an ideal system to use in such an analysis.
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It is now well established that at least some teleosts have a directional hearing sense (see Schuijf and Buwalda 1980). The cod, Gadus morhua, detects a change in the direction of propagation of sound and can discriminate between spatially separated sound sources, both in the horizontal and median vertical planes (Chapman and Johnstone 1974, Schuijf 1975, Hawkins and Sand 1977). Indeed, cod can discriminate between frontally incident and caudally incident sound waves (Schuijf and Buwalda 1975) and even distinguish between diametrically opposed sound sources in both the median vertical and transverse vertical planes (Buwalda, Schuijf, and Hawkins 1981). Thus, the cod discriminates direction in circumstances that are ambiguous or confusing for man, whose directional capabilities in the median vertical plane are poor (Butler 1974).
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Under the described experimental conditions vibration responses were recorded to stimulus frequencies extending rarely higher than 120 cyc
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