Fast Reverse Propagation of Sound in the Living Cochlea

The auditory sensory organ, the cochlea, not only detects but also generates sounds. Such sounds, otoacoustic emissions, are widely used for diagnosis of hearing disorders and to estimate cochlear nonlinearity. However, the fundamental question of how the otoacoustic emission exits the cochlea remains unanswered. In this study, emissions were provoked by two tones with a constant frequency ratio, and measured as vibrations at the basilar membrane and at the stapes, and as sound pressure in the ear canal. The propagation direction and delay of the emission were determined by measuring the phase difference between basilar membrane and stapes vibrations. These measurements show that cochlea-generated sound arrives at the stapes earlier than at the measured basilar membrane location. Data also show that basilar membrane vibration at the emission frequency is similar to that evoked by external tones. These results conflict with the backward-traveling-wave theory and suggest that at low and intermediate sound levels, the emission exits the cochlea predominantly through the cochlear fluids.     

Scaring seals by sound

In 1974 and 1975 a series of trials were made to investigate the effectiveness of sound as a deterrent to marauding seals at salmon netting stations. A feasibility trial was followed by experimental work on a captive juvenile Common seal. A wide variety of sounds including pure tones, Killer whale calls and recorded loud noises were transmitted and responses were recorded on videotape. While one sound appeared to elicit an alarm reaction, habituation was rapid. Field trials were carried out at netting stations at the mouth of the River Tweed which frequently suffer damage from Grey seals. Although the frequencies used spanned the entire hearing range of seals, no sound was consistently effective in scaring seals from the nets. It is concluded that the prospect of an acoustic deterrent is remote.     

Activation of Auditory Cortex by Anticipating and Hearing Emotional Sounds: An MEG Study

To study how auditory cortical processing is affected by anticipating and hearing of long emotional sounds, we recorded auditory evoked magnetic fields with a whole-scalp MEG device from 15 healthy adults who were listening to emotional or neutral sounds. Pleasant, unpleasant, or neutral sounds, each lasting for 6 s, were played in a random order, preceded by 100-ms cue tones (0.5, 1, or 2 kHz) 2 s before the onset of the sound. The cue tones, indicating the valence of the upcoming emotional sounds, evoked typical transient N100m responses in the auditory cortex. During the rest of the anticipation period (until the beginning of the emotional sound), auditory cortices of both hemispheres generated slow shifts of the same polarity as N100m. During anticipation, the relative strengths of the auditory-cortex signals depended on the upcoming sound: towards the end of the anticipation period the activity became stronger when the subject was anticipating emotional rather than neutral sounds. During the actual emotional and neutral sounds, sustained fields were predominant in the left hemisphere for all sounds. The measured DC MEG signals during both anticipation and hearing of emotional sounds implied that following the cue that indicates the valence of the upcoming sound, the auditory-cortex activity is modulated by the upcoming sound category during the anticipation period.     

Sounds of shallow water fishes pitch within the quiet window of the habitat ambient noise

The habitat ambient noise may exert an important selective pressure on frequencies used in acoustic communication by animals. A previous study demonstrated the presence of a match between the low-frequency quiet region of the stream ambient noise (termed ‘quiet window’) and the main frequencies used for sound production and hearing by two stream gobies (Padogobius bonelli, Gobius nigricans). The present study examines the spectral features of ambient noise in very shallow freshwater, brackish and marine habitats and correlates them to the range of dominant frequencies of sounds used by nine species of Mediterranean gobies reproducing in these environments. Ambient noise spectra of these habitats featured a low-frequency quiet window centered at 100 Hz (stream, sandy/rocky sea shore), or at 200 Hz (spring, brackish lagoon). The analysis of the ambient noise/sound spectrum relationships showed the sound frequencies matched the frequency band of the quiet window in the ambient noise typical of their own habitat. Analogous ambient noise/sound frequency relationships were observed in other shallow-water teleosts living in similar underwater environments. Conclusions may be relevant to the understanding of evolution of fish acoustic communication and hearing.     

Neural representation of the acoustic biotope

Cats were stimulated with tones and with natural sounds selected from the normal acoustic environment of the animal. Neural activity evoked by the natural sounds and tones was recorded in the cochlear nucleus and in the medial geniculate body. The set of biological sounds proved to be effective in influencing neural activity of single cells at both levels in the auditory system. At the level of the cochlear nucleus the response of a neuron evoked by a natural sound stimulus could be understood reasonably well on the basis of the structure of the spectrograms of the natural sounds and the unit's responses to tones. At the level of the medial geniculate body analysis with tones did not provide sufficient information to explain the responses to natural sounds. At this level the use of an ensemble of natural sound stimuli allows the investigation of neural properties, which are not seen by analysis with simple artificial stimuli. Guidelines for the construction of an ensemble of complex natural sound stimuli, based on the ecology and ethology of the animal under investigation are discussed. This stimulus ensemble is defined as the Acoustic Biotope.     

Awareness reactions and avoidance responses to sound in juvenile Atlantic salmon, Salmo salar L.

The possibility of using intense sound as a deterrent for juvenile Atlantic salmon ( Sulmo salar L. ) was studied by recording both physiological awareness reactions in an acoustic tube and behavioural avoidance responses in a pool. The measured awareness reactions consisted of decreased heart rate and breathing movements. Three criteria for the awareness reaction were used to compare the effect of different frequencies between 5 and 150 Hz: (i) threshold for spontaneous awareness reactions relative to the hearing thresholds, (ii) magnitude of the change in heart rate, (iii) degree of habituation to sound. After these criteria the lowest frequencies (5–10 Hz) were most effective in eliciting an awareness reaction from the fish. The responses of freely swimming fish to 10 and 150 Hz sounds were studied in an artificial pool. Juvenile salmon showed avoidance responses to 10 Hz stimulation at intensities 10–15 dB above the threshold for spontaneous awareness reactions measured in the acoustic tube. The 150 Hz sound failed to evoke avoidance responses, even at a level 30 dB above the threshold for spontaneous awareness reactions.     

褐菖鲉的听觉阈值研究

利用听觉诱发电位记录技术研究了褐菖鲉(Sebasticus marmoratus)的听觉阈值。通过采用听觉生理系统记录和分析了8尾褐菖鲉对频率范围在100—1000 Hz的7种不同频率的声音刺激的诱发电位反应。结果表明, 褐菖鲉的听觉阈值在整体上随着频率增加而增加, 对100—300 Hz的低频声音信号敏感, 最敏感频率为150 Hz, 对应的听觉阈值为70 dB re 1 μPa。褐菖鲉的听觉敏感区间与其发声频率具有较高的匹配性, 表明其声讯交流的重要性。同时, 人为低频噪声可能对其声讯交流造成影响。     

An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes

Fishes use a variety of sensory systems to learn about their environments and to communicate. Of the various senses, hearing plays a particularly important role for fishes in providing information, often from great distances, from all around these animals. This information is in all three spatial dimensions, often overcoming the limitations of other senses such as vision, touch, taste and smell. Sound is used for communication between fishes, mating behaviour, the detection of prey and predators, orientation and migration and habitat selection. Thus, anything that interferes with the ability of a fish to detect and respond to biologically relevant sounds can decrease survival and fitness of individuals and populations. Since the onset of the Industrial Revolution, there has been a growing increase in the noise that humans put into the water. These anthropogenic sounds are from a wide range of sources that include shipping, sonars, construction activities (e.g., wind farms, harbours), trawling, dredging and exploration for oil and gas. Anthropogenic sounds may be sufficiently intense to result in death or mortal injury. However, anthropogenic sounds at lower levels may result in temporary hearing impairment, physiological changes including stress effects, changes in behaviour or the masking of biologically important sounds. The intent of this paper is to review the potential effects of anthropogenic sounds upon fishes, the potential consequences for populations and ecosystems and the need to develop sound exposure criteria and relevant regulations. However, assuming that many readers may not have a background in fish bioacoustics, the paper first provides information on underwater acoustics, with a focus on introducing the very important concept of particle motion, the primary acoustic stimulus for all fishes, including elasmobranchs. The paper then provides background material on fish hearing, sound production and acoustic behaviour. This is followed by an overview of what is known about effects of anthropogenic sounds on fishes and considers the current guidelines and criteria being used world-wide to assess potential effects on fishes. Most importantly, the paper provides the most complete summary of the effects of anthropogenic noise on fishes to date. It is also made clear that there are currently so many information gaps that it is almost impossible to reach clear conclusions on the nature and levels of anthropogenic sounds that have potential to cause changes in animal behaviour, or even result in physical harm. Further research is required on the responses of a range of fish species to different sound sources, under different conditions. There is a need both to examine the immediate effects of sound exposure and the longer-term effects, in terms of fitness and likely impacts upon populations.     

摄食声对草鱼幼鱼的诱集作用

以草鱼(Ctenopharyngodon idellus)幼鱼为实验对象,进行了声音播放实验,旨在探究草鱼幼鱼对水下录制的草鱼摄食浮萍声音(简称摄食声)的行为反应。以不播放声音的草鱼鱼群作为对照,探讨了4种单频音(500、1000、2000和3000 Hz)和摄食声对草鱼游泳行为和在水槽内的分布的影响。结果表明:在播放单频音时, 3min内草鱼的趋音游泳速度和逗留时间与对照组无显著性差异(P>0.05);在播放摄食声时, 3min内草鱼的趋音游泳速度和逗留时间显著高于4种单频音组和对照组(P<0.05);在播放单频音时, 20min内草鱼的平均游泳速度、水槽内的分布和趋音率与对照组无显著性差异(P>0.05);在播放摄食声时, 20min内草鱼的平均游泳速度和趋音率都显著高于4种单频音组和对照组(P<0.05)。草鱼摄食声对草鱼幼鱼有诱集作用,为声音诱鱼技术研究提供了科学依据。     

The psychophysics of concurrent sound segregation.

To perceptually separate concurrent complex sounds, normally hearing listeners simultaneously combine information across a wide range of frequency components. Three psychoacoustical experiments are described which investigate different forms of this across-frequency processing. The first two experiments investigate the role of coherence of frequency modulation (FM) between widely separated frequency components of a complex sound. The first experiment bolsters existing evidence that, for harmonic sounds, listeners can discriminate coherent from incoherent FM, but only by detecting the mistuning that arises from incoherent FM. The second demonstrates that, for inharmonic sounds, coherence of FM has no effect on the phenomenon of modulation detection interference (see Moore & Shailer, this symposium) once within-channel cues (combination tones and beating) are masked by background noise. It is concluded that there is not an across-frequency mechanism specific to the detection of FM incoherence. The third experiment investigates the extent to which the detection of mistuning of one component of a harmonic complex is impaired by an interfering sound (the 'interferer') with a frequency spectrum similar to that of the mistuned component. When the interferer is gated on and off with the harmonic complex, it has only a small effect provided that its level is more than 3 dB below that of the target. However, when the interferer starts before and ends after the complex, thresholds are elevated more, and this elevation occurs even for low-level interferers. Explanations of this effect in terms of adaptation and of auditory streaming are discussed.     

Effects of temperature on sound production and auditory abilities in the Striped Raphael catfish Platydoras armatulus (Family Doradidae)

Background

Sound production and hearing sensitivity of ectothermic animals are affected by the ambient temperature. This is the first study investigating the influence of temperature on both sound production and on hearing abilities in a fish species, namely the neotropical Striped Raphael catfish Platydoras armatulus.

Methodology/Principal Findings

Doradid catfishes produce stridulation sounds by rubbing the pectoral spines in the shoulder girdle and drumming sounds by an elastic spring mechanism which vibrates the swimbladder. Eight fish were acclimated for at least three weeks to 22°, then to 30° and again to 22°C. Sounds were recorded in distress situations when fish were hand-held. The stridulation sounds became shorter at the higher temperature, whereas pulse number, maximum pulse period and sound pressure level did not change with temperature. The dominant frequency increased when the temperature was raised to 30°C and the minimum pulse period became longer when the temperature decreased again. The fundamental frequency of drumming sounds increased at the higher temperature. Using the auditory evoked potential (AEP) recording technique, the hearing thresholds were tested at six different frequencies from 0.1 to 4 kHz. The temporal resolution was determined by analyzing the minimum resolvable click period (0.3–5 ms). The hearing sensitivity was higher at the higher temperature and differences were more pronounced at higher frequencies. In general, latencies of AEPs in response to single clicks became shorter at the higher temperature, whereas temporal resolution in response to double-clicks did not change.

Conclusions/Significance

These data indicate that sound characteristics as well as hearing abilities are affected by temperatures in fishes. Constraints imposed on hearing sensitivity at different temperatures cannot be compensated even by longer acclimation periods. These changes in sound production and detection suggest that acoustic orientation and communication are affected by temperature changes in the neotropical catfish P. armatulus.     

Sound production, hearing and possible interception under ambient noise conditions in the topmouth minnow Pseudorasbora parva

Sounds were produced by the topmouth minnow Pseudorasbora parva , a common Eurasian cyprinid, during feeding but not during intraspecific interactions. Feeding sounds were short broadband pulses with main energies between 100 and 800 Hz. They varied in their characteristics (number of single sounds per feeding sequence, sound duration and period, and sound pressure level) depending on the food type (chironomid larvae, Tubifex worms and flake food). The loudest sounds were emitted when food was taken up at the water surface, most probably reflecting 'suctorial' feeding. Auditory sensitivities were determined between 100 and 4000 Hz utilizing the auditory evoked potentials recording technique. Under laboratory conditions and in the presence of natural ambient noise recorded in Lake Neusiedl in eastern Austria, best hearing sensitivities were between 300 and 800 Hz (57 dB re 1 μPa v . 72 dB in the presence of ambient noise). Threshold-to-noise ratios were positively correlated to the sound frequency. The correlation between sound spectra and auditory thresholds revealed that P. parva can detect conspecific sounds up to 40 cm distance under ambient noise conditions. Thus, feeding sounds could serve as an auditory cue for the presence of food during foraging.     

Interspecific variation in the response of fish to anthropogenic noise

1. Elevated levels of anthropogenic noise, especially those observed through boating activity, can negatively impact fish species, but it remains unclear which species are most affected and which behavioural metrics are best used in assessing fish responses to underwater noise. The effects of boat sounds on freshwater species are of particular interest because freshwater environments are less studied than the marine realm despite comparably high levels of biodiversity.
2. In the current study, we examine the behavioural responses to boat noise in two freshwater species that differ in their hypothesised response to sound inputs: the spottail shiner (Notropis hudsonius), a species with known hearing specialisations, and the bluegill sunfish (Lepomis macrochirus), a species with more generalised hearing capabilities. Fish were presented with boat noise in a laboratory setting, and their swimming, escape and foraging behaviours were assessed to examine differential responses in relation to hypothesised hearing abilities.
3. Both species showed a decrease in general swimming behaviours but an increase in erratic movements in response to boat noise, indicative of stress responses for both species. Despite the similarities in response based on swimming behaviours however, only spottail shiners exhibited true escape responses to the onset of the noise stimulus, suggesting a more extreme reaction in the species with a more refined hearing ability.
4. Taken together, these results show that freshwater fish can respond to increased levels of anthropogenic noise, but that the severity of the response may differ based on auditory structures and therefore presumed hearing ability. The differences seen between behavioural metrics used (swimming vs. escape responses) also demonstrate how care must be taken in choosing a metric when developing exposure guidelines for underwater sound exposures, as different metrics could lead to differential impact assessments.

     

Sex-Specific Differences in Agonistic Behaviour,Sound Production and Auditory Sensitivity in the Callichthyid Armoured Catfish Megalechis thoracata

Background

Data on sex-specific differences in sound production, acoustic behaviour and hearing abilities in fishes are rare. Representatives of numerous catfish families are known to produce sounds in agonistic contexts (intraspecific aggression and interspecific disturbance situations) using their pectoral fins. The present study investigates differences in agonistic behaviour, sound production and hearing abilities in males and females of a callichthyid catfish.

Methodology/Principal Findings

Eight males and nine females of the armoured catfish Megalechis thoracata were investigated. Agonistic behaviour displayed during male-male and female-female dyadic contests and sounds emitted were recorded, sound characteristics analysed and hearing thresholds measured using the auditory evoked potential (AEP) recording technique. Male pectoral spines were on average 1.7-fold longer than those of same-sized females. Visual and acoustic threat displays differed between sexes. Males produced low-frequency harmonic barks at longer distances and thumps at close distances, whereas females emitted broad-band pulsed crackles when close to each other. Female aggressive sounds were significantly shorter than those of males (167 ms versus 219 to 240 ms) and of higher dominant frequency (562 Hz versus 132 to 403 Hz). Sound duration and sound level were positively correlated with body and pectoral spine length, but dominant frequency was inversely correlated only to spine length. Both sexes showed a similar U-shaped hearing curve with lowest thresholds between 0.2 and 1 kHz and a drop in sensitivity above 1 kHz. The main energies of sounds were located at the most sensitive frequencies.

Conclusions/Significance

Current data demonstrate that both male and female M. thoracata produce aggressive sounds, but the behavioural contexts and sound characteristics differ between sexes. Sexes do not differ in hearing, but it remains to be clarified if this is a general pattern among fish. This is the first study to describe sex-specific differences in agonistic behaviour in fishes.     

R-weighting provides better estimation for rat hearing sensitivity

Since sounds may induce physiological and behavioural changes in animals, it is necessary to assess and define the acoustic environment in laboratory animal facilities. Sound studies usually express sound levels as unweighted linear sound pressure levels. However, because a linear scale does not take account of hearing sensitivity-which may differ widely both between and within species at various frequencies-the results may be spurious. In this study a novel sound pressure level weighting for rats, R-weighting, was calculated according to a rat's hearing sensitivity. The sound level of a white noise signal was assessed using R-weighting, with H-weighting tailored for humans, A-weighting and linear sound pressure level combined with the response curves of two different loudspeakers. The sound signal resulted in different sound levels depending on the weighting and the type of loudspeaker. With a tweeter speaker reproducing sounds at high frequencies audible to a rat, R- and A-weightings gave similar results, but the H-weighted sound levels were lower. With a middle-range loudspeaker, unable to reproduce high frequencies, R-weighted sound showed the lowest sound levels. In conclusion, without a correct weighting system and proper equipment, the final sound level of an exposure stimulus can differ by several decibels from that intended. To achieve reliable and comparable results, standardization of sound experiments and assessment of the environment in animal facilities is a necessity. Hence, the use of appropriate species-specific sound pressure level weighting is essential. R-weighting for rats in sound studies is recommended.     

Acoustic communication in two freshwater gobies: the relationship between ambient noise,hearing thresholds and sound spectrum

Two freshwater gobies Padogobius martensii and Gobius nigricans live in shallow (5-70 cm) stony streams, and males of both species produce courtship sounds. A previous study demonstrated high noise levels near waterfalls, a quiet window in the noise around 100 Hz at noisy locations, and extremely short-range propagation of noise and goby signals. To investigate the relationship of this acoustic environment to communication, we determined audiograms for both species and measured parameters of courtship sounds produced in the streams. We also deflated the swimbladder in P. martensii to determine its effect on frequency utilization in sound production and hearing. Both species are maximally sensitive at 100 Hz and produce low-frequency sounds with main energy from 70 to 100-150 Hz. Swimbladder deflation does not affect auditory threshold or dominant frequency of courtship sounds and has no or minor effects on sound amplitude. Therefore, both species utilize frequencies for hearing and sound production that fall within the low-frequency quiet region, and the equivalent relationship between auditory sensitivity and maximum ambient noise levels in both species further suggests that ambient noise shapes hearing sensitivity.     

The hearing abilities of the prawn Palaemon serratus

The mechanism of sound reception and the hearing abilities of the prawn (Palaemon serratus) have been studied using a combination of anatomical, electron microscopic and electrophysiological approaches, revealing that P. serratus is responsive to sounds ranging in frequency from 100 to 3000 Hz. It is the first time that the Auditory Brainstem Response (ABR) recording technique has been used on invertebrates, and the acquisition of hearing ability data from the present study adds valuable information to the inclusion of an entire sub-phylum of animals when assessing the potential impact of anthropogenic underwater sounds on marine organisms. Auditory evoked potentials were acquired from P. serratus, using two subcutaneous electrodes positioned in the carapace close to the supraesophageal ganglion and the statocyst (a small gravistatic organ located below the eyestalk on the peduncle of the bilateral antennules). The morphology of the statocyst receptors and the otic nerve pathways to the brain have also been studied, and reveal that P. serratus possesses an array of sensory hairs projecting from the floor of the statocyst into a mass of sand granules embedded in a gelatinous substance. It is the purpose of this work to show that the statocyst is responsive to sounds propagated through water from an air mounted transducer. The fundamental measure of the hearing ability of any organism possessing the appropriate receptor mechanism is its audiogram, which presents the lowest level of sound that the species can hear as a function of frequency. The statocyst of P. serratus is shown here to be sensitive to the motion of water particles displaced by low-frequency sounds ranging from 100 Hz up to 3000 Hz, with a hearing acuity similar to that of a generalist fish. Also, recorded neural waveforms were found to be similar in both amplitude and shape to those acquired from fish and higher vertebrates, when stimulated with low-frequency sound, and complete ablation of the electrophysiological response was achieved by removal of the statocyst.     

The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2-5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.     

How Nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes

Nearly all demersal teleost marine fishes have pelagic larval stages lasting from several days to several weeks, during which time they are subject to dispersal. Fish larvae have considerable swimming abilities, and swim in an oriented manner in the sea. Thus, they can influence their dispersal and thereby, the connectivity of their populations. However, the sensory cues marine fish larvae use for orientation in the pelagic environment remain unclear. We review current understanding of these cues and how sensory abilities of larvae develop and are used to achieve orientation with particular emphasis on coral-reef fishes. The use of sound is best understood; it travels well underwater with little attenuation, and is current-independent but location-dependent, so species that primarily utilize sound for orientation will have location-dependent orientation. Larvae of many species and families can hear over a range of ~100-1000 Hz, and can distinguish among sounds. They can localize sources of sounds, but the means by which they do so is unclear. Larvae can hear during much of their pelagic larval phase, and ontogenetically, hearing sensitivity, and frequency range improve dramatically. Species differ in sensitivity to sound and in the rate of improvement in hearing during ontogeny. Due to large differences among-species within families, no significant differences in hearing sensitivity among families have been identified. Thus, distances over which larvae can detect a given sound vary among species and greatly increase ontogenetically. Olfactory cues are current-dependent and location-dependent, so species that primarily utilize olfactory cues will have location-dependent orientation, but must be able to swim upstream to locate sources of odor. Larvae can detect odors (e.g., predators, conspecifics), during most of their pelagic phase, and at least on small scales, can localize sources of odors in shallow water, although whether they can do this in pelagic environments is unknown. Little is known of the ontogeny of olfactory ability or the range over which larvae can localize sources of odors. Imprinting on an odor has been shown in one species of reef-fish. Celestial cues are current- and location-independent, so species that primarily utilize them will have location-independent orientation that can apply over broad scales. Use of sun compass or polarized light for orientation by fish larvae is implied by some behaviors, but has not been proven. Use of neither magnetic fields nor direction of waves for orientation has been shown in marine fish larvae. We highlight research priorities in this area.