The overlapping roles of the inner ear and lateral line: the active space of dipole source detection

The problems associated with the detection of sounds and other mechanical disturbances in the aquatic environment differ greatly from those associated with airborne sounds. The differences are primarily due to the incompressibility of water and the corresponding increase in importance of the acoustic near field. The near field, or hydrodynamic field, is characterized by steep spatial gradients in pressure, and detection of the accelerations associated with these gradients is performed by both the inner ear and the lateral line systems of fishes. Acceleration-sensitive otolithic organs are present in all fishes and provide these animals with a form of inertial audition. The detection of pressure gradients, by both the lateral line and inner ear, is the taxonomically most widespread mechanism of sound-source detection amongst vertebrates, and is thus the most likely primitive mode of detecting sound sources. Surprisingly, little is known about the capabilities of either the lateral line or the otolithic endorgan in the detection of vibratory dipole sources. Theoretical considerations for the overlapping roles of the inner ear and lateral line systems in midwater predict that the lateral line will operate over a shorter distance range than the inner ear, although with a much greater spatial resolution. Our empirical results of dipole detection by mottled sculpin, a benthic fish, do not agree with theoretical predictions based on midwater fishes, in that the distance ranges of the two systems appear to be approximately equal. This is almost certainly as a result of physical coupling between the fishes and the substrate. Thus, rather than having a greater active range, the inner ear appears to have a reduced distance range in benthic fishes, and the lateral line distance range may be concomitantly extended.     

Brainstem lateral line responses to sinusoidal wave stimuli in the goldfish, Carassius auratus

Extracellular recordings were made from single lateral line units in the medial octavolateralis nucleus in the brainstem of goldfish, Carassius auratus. Units were defined as receiving lateral line input if they responded to the water motions generated by a stationary, sinusoidally oscillating sphere and/or a moving sphere but not to airborne sound and vibrations. Units which responded to airborne sound or vibrations were assumed to receive input from the inner ear and were not further investigated. Responses of lateral line units were quantified in terms of the number of evoked spikes and the degree of phase-locking to a 50 Hz vibrating sphere presented at various stationary locations along the side of the fish. Receptive fields were characterized based on spike rate, degree of phase-locking and average phase angle as a function of sphere location. Four groups of units were distinguished: 1, units with receptive fields comparable to those of primary afferents; 2, units with receptive fields which consisted of one excitatory and one inhibitory area; 3, units with receptive fields which consisted of more than two excitatory and/or inhibitory areas; 4, units with receptive fields which consisted of a single excitatory or a single inhibitory area. The receptive fields of most units were characterized by adjacent excitatory and inhibitory areas. This organization is reminiscent of excitatory-inhibitory receptive field organizations in other vertebrate sensory systems.     

A novel hearing specialization in the New Zealand bigeye,Pempheris adspersa

The New Zealand bigeye, Pempheris adspersa, is a nocturnal planktivore and has recently been found to be an active sound producer. The rostral end of the swim bladder lies adjacent to Baudelot''s ligament which spans between the bulla and the cleithrum bone of the pectoral girdle. The aim of this study was to use the auditory evoked potential technique to physiologically test the possibility that this structure provides an enhanced sensitivity to sound pressure in the bigeye. At 100 Hz, bigeye had hearing sensitivity similar to that of goldfish (species with a mechanical connection between the swim bladder and the inner ear mediated by the Weberian ossicles) and were much more sensitive than other teleosts without ancillary hearing structures. Severing Baudelot''s ligament bilaterally resulted in a marked decrease in hearing sensitivity, as did swim bladder puncture or lateral line blockage. These results show that bigeye have an enhanced sensitivity to sound pressure and provide experimental evidence that the functional basis of this sensitivity represents a novel hearing specialization in fish involving the swim bladder, Baudelot''s ligament and the lateral line.     

Lateral line reception in still- and running water

The lateral line of fish is composed of neuromasts used to detect water motions. Neuromasts occur as superficial neuromasts on the skin and as canal neuromasts in subepidermal canals. Fibres of the lateral line nerves innervate both. There have been extensive studies on the responses of lateral line nerve fibres to dipole stimuli applied in still water. However, despite the fact that many fish live in rivers and/or swim constantly, responses of lateral line nerve fibres to dipole stimuli presented in running water have never been recorded. We investigated how the peripheral lateral line of still water fish ( Carassius auratus) and riverine fish ( Oncorhynchus mykiss) responds to minute sinusoidal water motions while exposed to unidirectional water flow. Both goldfish and trout have two types of posterior lateral line nerve fibres: Type I fibres, which most likely innervate superficial neuromasts, were stimulated by running water (10 cm s(-1)). The responses of type I fibres to water motions generated by a vibrating sphere were masked if the fish was exposed to running water. Type II fibres, which most likely innervate canal neuromasts, were not stimulated by running water. Consequently, responses of type II fibres to a vibrating sphere were not masked under flow conditions.     

Hair cell heterogeneity and ultrasonic hearing: recent advances in understanding fish hearing

The past decade has seen a wealth of new data on the auditory capabilities and mechanisms of fishes. We now have a significantly better appreciation of the structure and function of the auditory system in fishes with regard to their peripheral and central anatomy, physiology, behaviour, sound source localization and hearing capabilities. This paper deals with two of the newest of these findings, hair cell heterogeneity and the detection of ultrasound. As a result of this recent work, we now know that fishes have several different types of sensory hair cells in both the ear and lateral line and there is a growing body of evidence to suggest that these hair cell types arose very early in the evolution of the octavolateralis system. There is also some evidence to suggest that the differences in the hair cell types have functional implications for the way the ear and lateral line of fishes detect and process stimuli. Behavioural studies have shown that, whereas most fishes can only detect sound to 1-3 kHz, several species of the genus Alosa (Clupeiformes, i.e. herrings and their relatives) can detect sounds up to 180 kHz (or even higher). It is suggested that this capability evolved so that these fishes can detect one of their major predators, echolocating dolphins. The mechanism for ultrasound detection remains obscure, though it is hypothesized that the highly derived utricle of the inner ear in these species is involved.     

Coping with flow: behavior, neurophysiology and modeling of the fish lateral line system

With the mechanosensory lateral line fish perceive water motions relative to their body surface and local pressure gradients. The lateral line plays an important role in many fish behaviors including the detection and localization of dipole sources and the tracking of prey fish. The sensory units of the lateral line are the neuromasts which are distributed across the surface of the animal. Water motions are received and transduced into neuronal signals by the neuromasts. These signals are conveyed by afferent nerve fibers to the fish brain and processed by lateral line neurons in parts of the brainstem, cerebellum, midbrain, and forebrain. In the cerebellum, midbrain, and forebrain, lateral line information is integrated with sensory information from other modalities. The present review introduces the peripheral morphology of the lateral line, and describes our understanding of lateral line physiology and behavior. It focuses on recent studies that have investigated: how fish behave in unsteady flow; what kind of sensory information is provided by flow; and how fish use and process this information. Finally, it reports new theoretical and biomimetic approaches to understand lateral line function.     

Structure and Function of the Elasmobranch Auditory System

Behavioral evidence indicates that sharks detect underwatersound at frequencies up to 1000 Hz, and that certain low frequencysignals attract sharks from large distances. It appears thatthe adequate stimulus for "sound detecting" systems of the sharkis panicle motion, as opposed to fluctuations in sound pressure.The elasmobranch ear consists of the three semi-circular canalsfor detecting angular accelerations, and otolith organs fordetecting linear motion and accelerations due to gravity. Twoof these organs, the sacculus and macula neglecta, have beenshown to be responsive to vibratory motion, with the maculaneglecta having best sensitivity to vertical movements. A directvibrational pathway exists to the macula neglecta from the parietalfossa of the dorsal chondrocranium. It is not clear at present,however, whether it is the inner ear or the lateral line systemwhich is responsible for hearing. Both detection systems aretheoretically capable of providing information to the brainabout sound source location using non-parallel arrays of directionallysensitive hair-cell receptors. Recent theories of underwatersound localization by fishes and sharks suggest that the abilityto detect a vertical displacement component of an acoustic signal(e. g., via the macula neglecta) is necessary for instantaneouslocation decisions. It is not known, however, whether the sharkslocalize by processing information about various aspects ofthe sound field simultaneously (in parallel), or whether thesound field is sampled successively at different points in space.Clearly, more experimental work on the physiology of elasmobranchacoustic behavior is called for.     

Sea snakes (Lapemis curtus) are sensitive to low-amplitude water motions

The sea snake Lapemis curtus is a piscivorous predator that hunts at dusk. Like land snakes, sea snakes have scale sensillae that may be mechanoreceptive, i.e. that may be useful for the detection of water motions produced by prey fish. In addition, inner ear hair cells of sea snakes may also be involved in the detection of hydrodynamic stimuli. We generated water motions and pressure fluctuations with a vibrating sphere. In the test range 50-200 Hz evoked potentials were recorded from the midbrain of L. curtus in response to vibrating sphere stimuli. In terms of water displacement the lowest threshold amplitudes were in the frequency range 100-150 Hz. In this range peak-to-peak water displacement amplitudes of 1.8 microm (at 100 Hz) and 2.0 microm (150 Hz) generated a neural response in the most sensitive animal. Although this low sensitivity may be sufficient for the detection of fish-generated water motions, it makes it unlikely that L. curtus has a special hydrodynamic sense.     

Sensory processing of water currents by fishes

Water currents are extremely important in the aquatic environment and play a very significant role in the lives of fishes. Sensory processing of water currents involves a number of sensory modalities including the inner ear, vision, tactile sense and the mechanosensory lateral line. The inner ear will detect whole-body accelerations generated by changes in flow, or by turbulence, whereas visual and tactile inputs will signal translational movement with respect to an external visual or tactile reference frame. The superficial neuromasts of the mechanosensory lateral line detect flow over the surface of the body and have the appropriate anatomical distribution and physiological properties to signal the strength and the direction of flow and, hence, contribute to the detection of regional differences in flow over different parts of the body.     

The puzzle of hydrodynamic information processing: how are complex water motions analyzed by the lateral line?

We studied the discharges of neurons in the ascending lateral line pathway in response to the complex water motions generated by a moving object. The wave stimulus generated by the object was monitored with a hot-wire anemometer and with a custom-built particle imaging system. Responses of central lateral line neurons differ from those of primary afferent fibers in aspects like temporal discharge patterns and directional sensitivity. The data are consistent with the hypothesis that central lateral line neurons integrate input from many afferents innervating neuromasts distributed across large portions of the body surface.     

Sensory integration in the hydrodynamic world of rainbow trout

Water movements, of both abiotic and biotic origin, provide a wealth of information for fishes. They detect these water movements by arrays of hydrodynamic sensors located on the surface of the body as superficial neuromasts and embedded in subdermal lateral line canals. Recently, the anatomical dichotomy between superficial and canal neuromasts has been matched by demonstrations of a corresponding functional dichotomy. Superficial neuromasts are sensitive to water flows over the surface of the fish and are the sub-modality that participates in orientation to water currents, a behaviour known as rheotaxis. The canal neuromasts are sensitive to water vibration and it is this sub-modality that determines the localization of artificial prey. Recently, however, it has been shown that the complex behaviour of natural prey capture in the dark requires input from both lateral line sensory submodalities and here we show that the ability of trout to hold station behind a stationary object in fast flowing water also requires integration of information from both sub-modalities.     

Swim bladder and posterior lateral line nerve of the nurseryfish, Kurtus gulliveri (Perciformes: Kurtidae)

The morphology of the swim bladder and inner ear of the nurseryfish, Kurtus gulliveri, appear adapted for enhanced pressure wave reception. The saccule is enlarged and surrounded by very thin bone and two large fontanelles that would present reduced resistance to pressure waves. The swim bladder is elaborate, with six dorsolaterally projecting pairs of lobes that are tightly encased in ribs and an additional caudally projecting pair of lobes encased in the first hemal spine. The ribs and musculature surrounding the swim bladder laterally are very thin, so that four or five "rib windows" are readily apparent on back-lit specimens. This swim bladder-rib configuration would also present reduced resistance to pressure waves to enhance function as a peripheral auditory structure. However, high-resolution X-ray computed tomography and dissection reveal no anterior projections of the swim bladder that could serve as a mechanical coupling to the inner ear. The posterior lateral line nerve is well developed and lies directly over the tips of the ribs encasing the swim bladder lobes. This nerve is not, however, associated with a lateral line canal and a lateral line canal is absent on most of the body. We hypothesize that the posterior lateral line nerve transmits mechanosensory information from the swim bladder.     

压力波对听觉器官的致伤作用——Ⅰ.致伤部位和损伤特性

本工作用二十余种武器压力波源在不同暴露条件下对近二千只豚鼠进行了系统的致伤实验。结果表明,压力波暴露后致伤部位主要在中耳和内耳;即使压力峰值已高达190dBSPL,听觉中枢还未见有损伤迹象。中耳损伤和内耳损伤的程度都与压力波的强度有关,但两者并不平行,压力峰值大时压力波可以只损伤或主要损伤中耳,压力峰值不很大但重复发数较多或脉宽较大时,则可能只损伤或主要损伤内耳。在一定的条件下,中耳的损伤能缓冲压力波对内耳的冲击,从而减轻内耳的损伤。在中耳损伤或中耳、内耳混合损伤时,豚鼠的听力丧失并没有象在人的噪声性耳聋时(内耳损伤为主)常见的那种突出的高频选择性。     

Water wave discrimination in the surface-feeding fish Aplocheilus lineatus

The surface-feeding fish Aplocheilus lineatus uses its cephalic lateral line to detect water surface waves caused by prey insects. The ability of Aplocheilus to discriminate between surface waves with aid of the lateral line system was tested by go/no-go conditioning. Our results show that Aplocheilus can distinguish between single-frequency surface wave stimuli with equal velocity or equal acceleration amplitudes which differ only in frequency. Frequency difference limens were about 15%, i.e. fish distinguished a 20-Hz wave stimulus from a 23-Hz stimulus in 100% of the trials. Aplocheilus can also discriminate between pure sine-wave stimuli and sine waves which show abrupt frequency changes. In contrast, fish were unable to distinguish amplitude-modulated wave stimuli (carrier frequency 20, 40 and 60 Hz, modulation frequency 10 and 20 Hz) from pure sine waves of the same frequency, even if amplitude modulation depth was 80%. Accepted: 27 December 1996     

Two-dimensional receptive fields of midbrain lateral line units in the goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>

We determined the receptive fields of midbrain lateral line units in goldfish, Carassius auratus, with a 50 Hz vibrating sphere placed at various azimuths and elevations alongside the fish and studied how responses were affected by different directions of sphere vibration. The receptive fields of toral lateral line units, in contrast to those of primary afferent nerve fibers, did not represent the pressure gradient pattern generated by a vibrating sphere. Thus, unlike primary afferents, single toral lateral line units did not code for source location in their spatial discharge patterns. The two-dimensional receptive fields were round, horizontally or vertically stretched, or complex. While some toral lateral line units were sensitive to the direction of sphere vibration others were not.     

The amphibian octavo-lateralis system and its regressive and progressive evolution

The phylogenetic and ontogenetic changes in the octavolateralis system of sarcopterygian fish and tetrapods, presumed to be important for the formation of an amphibian auditory system, are reviewed. The lateral line system shows rudimentation of lines and loss of ampullary electroreceptors in many amphibians; in some amphibians it never develops. The metamorphic changes of the lateral-line system show different patterns in the different amphibian lineages with metamorphic retention in most urodeles and metamorphic loss in most anurans. The multitude of both ontogenetic and phylogenetic changes of the lateral line system among amphibians do exclude any prediction as to how this system might have changed in ancestral amniotes. The most important auditory epithelium of the tetrapod inner ear, the basilar papilla, seems to be primitively present in all tetrapods and Latimeria. In two amphibian lineages there is a trend towards rudimentation and loss of the basilar papilla. Only in the third order, the anurans, a tympanic ear develops and the inner ear shows a progressive evolution of the auditory epithelia. Together with the known differences in the periotic labyrinth of amphibians and amniotes, this scenario suggests a parallel evolution of the amniotic and anuran auditory periphery. All mechanoreceptive hair cells of the lateral line system and the inner ear appear to receive a common and bilateral efferent innervation. Among amphibians this pattern is represented only in some urodeles, whereas anurans show a derived pattern with loss of a bilateral component and presumably also of a common neuromast/inner ear component. Changes in the rhombencephalic nuclei which receive octavo-lateralis afferent fibers show a trend towards development of auditory nuclei only in the anuran lineage. The phylogenetic appearance of an auditory nucleus in this lineage coincides with the complete absence of formation of ampullary electroreceptors. In contrast, the earlier claim of a correlation between a metamorphic loss of the lateral line system and the formation of an auditory nucleus is not supported by more recent data: an auditory nucleus develops in anurans already prior to metamorphosis and is present in all anurans even when they retain the neuromast system. In anurans with a metamorphic loss of the neuromasts, the second order neurons degenerate as well. This independence of the auditory and the second order lateral line nuclei is further substantiated by their separate projection to other brain areas, like the torus semicircularis of the midbrain, and their functional properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

The responses of central octavolateralis cells to moving sources

Mechanosensory lateral line units recorded from the medulla (medial octavolateralis nucleus) and midbrain (torus semicircularis) of the bottom dwelling catfish Ancistrus sp. responded to water movements caused by an object that passed the fish laterally. In terms of peak spike rate or total number of spikes elicited responses increased with object speed and sometimes showed saturation (Figs. 7, 14). At sequentially greater distances the responses of most medullary lateral line units decayed with object distance (Fig. 11). Units tuned to a certain object speed or distance were not found. The signed directionality index of most lateral line units was between –50 and +50, i.e. these units were not or only slightly sensitive to the direction of object motion (Figs. 10, 17). However, some units were highly directionally sensitive in that the main features of the response histograms and/or peak spike rates clearly depended on the direction of object movement (e.g. Fig. 9C, D and Fig. 16). Midbrain lateral line units of Ancistrus may receive input from more than one sensory modality. All bimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. Units which receive bimodal input may show an extended speed range (e.g. Fig. 18).Abbreviations MON medial octavolateralis nucleus - MSR mean spike rate - PSR peak spike rate - p-p peak-to-peak - SDI signed directionality index     

Directionality of sound perception in the external ear of the dog

Sound pressure level of tone was measured using a probe tube microphone at entrance to the dog's external meatus as a function of the azimuth of the sound source. It was demonstrated that directionality of the dog's external ear and corresponding values of interaural intensity differences (delta I) were gradually increased as the tone frequency raised from 0.5 to 40 kHz. Transfer in pinnae locations from lateral to frontal positions (one of the components of orientation reaction to an unexpected sound) resulted in some narrowing of directionality diagrams and in a displacement of their maxima towards the head midline. It was calculated that owing to this effects the extent of monotonic part of the function relating delta I and azimuth of a source were enlarged. The lateral pinnae position was suggested to be optimal for sound detection and the frontal one for localization of the moving sound source.     

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

The ability to detect airborne sound is essential for many animals. Examples from the inner ear of mammals and bushcrickets demonstrate that similar detection strategies evolved in taxonomically distant species. Both mammalian and bushcricket ears possess a narrow strip of sensory tissue that exhibits an anatomical gradient and traveling wave motion responses used for frequency discrimination. We measured pressure and motion in the bushcricket ear to investigate physical properties, stiffness, and mass, which govern the mechanical responses to sound. As in the mammalian cochlea, sound-induced fluid pressure and motion responses were tonotopically organized along the longitudinal axis of the crista acustica, the bushcricket’s hearing organ. The fluid pressure at the crista and crista motion were used to calculate the acoustic impedance of the organ-bounded fluid mass (Z_mass). We used a theoretical wave analysis of wavelength data from a previous study to predict the crista acustica stiffness. The wave analysis also predicts Z_mass, and that result agreed reasonably well with the directly measured Z_mass, lending support to the theoretical wave analysis. The magnitude of the crista stiffness was similar to basilar membrane stiffness in mammals, and as in mammals, the stiffness decreased from the high-frequency to the low-frequency region. At a given location, the stiffness increased with increasing frequency, corresponding to increasing curvature of the traveling wave (decreasing wavelength), indicating that longitudinal coupling plays a substantial role in determining crista stiffness. This is in contrast to the mammalian ear, in which stiffness is independent of frequency and longitudinal coupling is relatively small.