Beaked whale auditory evoked potential hearing measurements

Several mass strandings of beaked whales have recently been correlated with military exercises involving mid-frequency sonar highlighting unknowns regarding hearing sensitivity in these species. We report the hearing abilities of a stranded juvenile beaked whale (Mesoplodon europaeus) measured with auditory evoked potentials. The beaked whale’s modulation rate transfer function (MRTF) measured with a 40-kHz carrier showed responses up to an 1,800 Hz amplitude modulation (AM) rate. The MRTF was strongest at the 1,000 and 1,200 Hz AM rates. The envelope following response (EFR) input–output functions were non-linear. The beaked whale was most sensitive to high frequency signals between 40 and 80 kHz, but produced smaller evoked potentials to 5 kHz, the lowest frequency tested. The beaked whale hearing range and sensitivity are similar to other odontocetes that have been measured.     

Auditory temporal resolution and evoked responses to pulsed sounds for the Yangtze finless porpoises (<Emphasis Type="Italic">Neophocaena phocaenoides asiaeorientalis</Emphasis>)

Temporal cues are important for some forms of auditory processing, such as echolocation. Among odontocetes (toothed whales, dolphins, and porpoises), it has been suggested that porpoises may have temporal processing abilities which differ from other odontocetes because of their relatively narrow auditory filters and longer duration echolocation signals. This study examined auditory temporal resolution in two Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) using auditory evoked potentials (AEPs) to measure: (a) rate following responses and modulation rate transfer function for 100 kHz centered pulse sounds and (b) hearing thresholds and response amplitudes generated by individual pulses of different durations. The animals followed pulses well at modulation rates up to 1,250 Hz, after which response amplitudes declined until extinguished beyond 2,500 Hz. The subjects had significantly better hearing thresholds for longer, narrower-band pulses similar to porpoise echolocation signals compared to brief, broadband sounds resembling dolphin clicks. Results indicate that the Yangtze finless porpoise follows individual acoustic signals at rates similar to other odontocetes tested. Relatively good sensitivity for longer duration, narrow-band signals suggests that finless porpoise hearing is well suited to detect their unique echolocation signals.     

Temporal resolution of the Florida manatee (<Emphasis Type="Italic">Trichechus manatus latirostris</Emphasis>) auditory system

Auditory evoked potential (AEP) measurements of two Florida manatees (Trichechus manatus latirostris) were measured in response to amplitude modulated tones. The AEP measurements showed weak responses to test stimuli from 4 kHz to 40 kHz. The manatee modulation rate transfer function (MRTF) is maximally sensitive to 150 and 600 Hz amplitude modulation (AM) rates. The 600 Hz AM rate is midway between the AM sensitivities of terrestrial mammals (chinchillas, gerbils, and humans) (80–150 Hz) and dolphins (1,000–1,200 Hz). Audiograms estimated from the input–output functions of the EPs greatly underestimate behavioral hearing thresholds measured in two other manatees. This underestimation is probably due to the electrodes being located several centimeters from the brain.     

Effects of saccular otolith removal on hearing sensitivity of the sleeper goby (<Emphasis Type="Italic">Dormitator latifrons</Emphasis>)

It is not known to what extent the entire saccule contributes to overall hearing sensitivity in any fish species. Here we report directional and frequency sensitivity in a teleost fish (Dormitator latifrons) and effects of unilateral and bilateral removal of saccular otoliths on its hearing sensitivity. The fish had different hearing thresholds in the horizontal (-54.4 to -50.3 dB re: 1 micro m) and mid-sagittal (-58.6 to -53.1 dB) planes. At 100 Hz, unilateral otolith removal did not significantly change hearing sensitivity in the mid-sagittal plane, but caused selective reductions of auditory sensitivity by 3-7 dB in the azimuthal axes that are consistent with the longitudinal axis of the damaged saccule. Along the fish's longitudinal axis, unilateral otolith removal significantly decreased auditory sensitivity at 50 Hz and 400 Hz, but not at 100 Hz, 200 Hz, and 345 Hz. At 100 Hz, bilateral otolith removal resulted in robust hearing loss of 27-35 dB at different axes in both horizontal and mid-sagittal planes. Along the fish's longitudinal axis, the bilateral removal reduced auditory sensitivity by 13-27 dB at the different frequencies. Therefore, these results demonstrate that the saccule plays important roles in directional hearing and frequency responses.     

Pacific herring hearing does not include ultrasound

Recent studies have shown that some clupeid fishes, including shad and menhaden, can detect ultrasound (sound with frequencies higher than 20 kHz) and actively avoid it. However, other clupeids, including sardines and anchovies, do not detect ultrasound. The hearing abilities of herring are of particular interest because of their commercial importance, our reliance on acoustics to monitor their populations and behavioural evidence of responses to high-frequency sound by some clupeid species. We measured the hearing sensitivity of Pacific herring (Clupea pallasii) using the auditory brainstem response and found that they were unable to detect ultrasonic signals at received levels up to 185 dB re 1 microPa. Herring had hearing thresholds at lower frequencies (100-5000 Hz) that were typical of other non-ultrasound-detecting clupeids. This lower-frequency hearing sensitivity could explain the results of several earlier studies showing responses to broadband sounds.     

Temporal modulation transfer functions in the barn owl (<Emphasis Type="Italic">Tyto alba</Emphasis>)

Barn owls (Tyto alba) have evolved several specializations in their auditory system to achieve the high sensory acuity required for prey capture, including superior processing of interaural time differences and phase coding in the auditory periphery. Here, we tested whether barn owls are capable of high temporal resolution that may be a prerequisite for the accuracy in binaural processing. Temporal resolution was measured psychoacoustically and demonstrated in temporal modulation transfer functions. Four barn owls were trained in an operant task with food reward to detect sinusoidal amplitude modulations within an 800-ms gated white-noise burst or 800-ms periods of modulation in continuous white noise (spectrum levels of -5 dB and 15 dB SPL). Within the range of tested amplitude modulation frequencies from 5 Hz to 1280 Hz, barn owls' detection thresholds were lowest at 10-20 Hz. This sensitivity corresponds to an intensity-difference limen of between 0.9 dB and 1.4 dB. For all conditions, temporal modulation transfer functions showed band-pass characteristics with a high-frequency cutoff in the range of 37 Hz to 92 Hz, corresponding to minimum integration times of 4.3 ms and 1.7 ms, respectively. In summary, these data indicate a temporal resolution in the owl's auditory system that is good, but not unusual, compared to other vertebrates.     

Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls

Absolute thresholds and critical masking ratios were determined behaviorally for the European barn owl (Tyto alba guttata). It shows an excellent sensitivity throughout its hearing range with a minimum threshold of −14.2 dB sound pressure level at 6.3 kHz, which is similar to the sensitivity found in the American barn owl (Tyto alba pratincola) and some other owls. Both the European and the American barn owl have a high upper-frequency limit of hearing exceeding that in other bird species. Critical masking ratios, that can provide an estimate for the frequency selectivity in the barn owl's hearing system, were determined with a noise of about 0 dB spectrum level. They increased from 19.1 dB at 2 kHz to 29.2 dB at 8 kHz at a rate of 5.1 dB per octave. The corresponding critical ratio bandwidths were 81, 218, 562 and 831 Hz for test-tone frequencies of 2, 4, 6.3 and 8 kHz, respectively. These values indicate, contrary to expectations based on the spatial representation of frequencies on the basilar papilla, increasing bandwidths of auditory filters in the region of the barn owl's auditory fovea. This increase, however, correlates with the increase in the bandwidths of tuning curves in the barn owl's auditory fovea. Accepted: 27 November 1997     

Temporal peculiarities of responses of auditory system neurons of the frog <Emphasis Type="Italic">Rana temporaria</Emphasis> to tone bursts with different modulation frequencies

Activity of medullar and midbrain auditory neurons at action of amplitude-modulated tone burst was recorded in immobilized common frogs Rana temporaria. Depth of modulation amounted to 10% or 80%, frequency of modulation varied from 5 to 150 Hz, and carrier intensity was in the range of 20–30 dB. Phasic neurons in medulla clearly reproduced the modulation frequency, but only at the 80% modulation depth. However, during presentation of signal with the 10% modulation depth, these neurons practically did not respond. Tonic neurons were able to reproduce the modulation frequency up to 10–150 Hz, but at the 10% modulation depth, the degree of reproduction of envelope was rather low, although for several first modulation periods it rose statistically significantly. In midbrain, the highest frequency of the reproduced modulation sharply fell. At greater modulation frequencies, the response of these neurons qualitatively reminds that of medullar neurons. At the low modulation frequencies, there is identified a group of midbrain neurons with a prominent increase of the signal modulation. This occurs in the frequency diapason up to 60 Hz; at an increase of the modulation frequency the time of achievement of maximal synchronization decreases. The optimal modulation frequency in many neurons of semicircular torus corresponds to parameters of the male nuptial call.     

Frequency tuning curves of the dolphin's hearing: envelope-following response study

Simultaneous tone-tone masking in conjunction with the envelope-following response (EFR) recording was used to obtain tuning curves in dolphins (Turslops truncatus). The EFR was evoked by amplitude-modulated probes of various frequencies. A modulation rate of 600 Hz was found to fit the requirement to have a narrow spectrum and evoke EFR of large amplitude. Tuning curves were obtained within the frequency range from 11.2 to 110 kHz. The Q₁₀ values of the obtained tuning curves varied from 12–14 at the 11.2 kHz center frequency to 17–20 at the 64–90 kHz frequencies.Abbreviations ABR auditory brainstem response - EFR envelope following response - ERB equivalent rectangular bandwidth     

Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera)

Females of the parasitoid fly Emblemasoma auditrix find their host cicada (Okanagana rimosa) by its acoustic signals. In laboratory experiments, fly phonotaxis had a mean threshold of about 66 dB SPL when tested with the cicada calling song. Flies exhibited a frequency dependent phonotaxis when testing to song models with different carrier frequencies (pulses of 6 ms duration and a repetition rate of 80 pulses s(-1)). However, the phonotactic threshold was rather broadly tuned in the range from 5 kHz to 11 kHz. Phonotaxis was also dependent on the temporal parameters of the song models: repetition rates of 60 pulses s(-1) and 80 pulses s and pulse durations of 5-7 ms resulted in the highest percentages of phonotaxis performing animals coupled with the lowest threshold values. Thus, parasitoid phonotaxis is adapted especially to the temporal parameters of the calling song of the host. Choice experiments revealed a preference of a song model with 9 kHz carrier frequency (peak energy of the host song) compared with 5 kHz carrier frequency (electrophysiologically determined best hearing frequency). However, this preference changed with the relative sound pressure level of both signals. When presented simultaneously, E. auditrix preferred 5-kHz signals, if they were 5 dB SPL louder than the 9-kHz signal.     

Electrophysiological responses in guinea pig cochlea to low frequency sound stimuli: distortion of cochlear microphonic (CM) wave form

The present experiment investigated whether or not auditory responses of the middle and/or inner ear in guinea pigs to low frequency sound stimuli [ 60 Hz-2 kHz at 90-120 dB(SPL) ] exhibited the harmonic distortion phenomenon resulting from cochlear microphonics (CM). Measurement of CM leading in turn I by the differential electrode recording method involved measurement of 50 microV isopotential responses, output voltages and CM wave form distortion at each constant sound pressure. The results obtained were as follows: (1) On the 50 microV isopotential response curve and the output voltage curves, the changes at 60-90 Hz were different from those at higher frequencies. (2) At stimuli of 90 or 100 dB(SPL), CM wave form distortion appeared frequently at frequencies below 120 Hz, but were less pronounced above approximately 200 Hz. (3) When raised to 110 and 120 dB(SPL), almost all CM wave forms were distorted at all test frequencies between 60 and 500 Hz. (4) The patterns of CM wave form distortion at frequencies below approximately 120 Hz showed peak clipping and triangular wave distortions, while those at frequencies above approximately 200 Hz showed little of these distortions.     

Audiogram of the chicken (Gallus gallus domesticus) from 2 Hz to 9 kHz

The pure-tone thresholds of four domestic female chickens were determined from 2 Hz to 9 kHz using the method of conditioned suppression/avoidance. At a level of 60 dB sound pressure level (re 20 μN/m²), their hearing range extends from 9.1 Hz to 7.2 kHz, with a best sensitivity of 2.6 dB at 2 kHz. Chickens have better sensitivity than humans for frequencies below 64 Hz; indeed, their sensitivity to infrasound exceeds that of the homing pigeon. However, when threshold testing moved to the lower frequencies, the animals required additional training before their final thresholds were obtained, suggesting that they may perceive frequencies below 64 Hz differently than higher frequencies.     

Perceptual interaction between carrier periodicity and amplitude-modulation in the gerbil (<Emphasis Type="Italic">Meriones unguiculatus</Emphasis>)

Due to its extended low-frequency hearing, the Mongolian gerbil (Meriones unguiculatus) has become a well-established animal model for human auditory processing. Here, two experiments are presented which quantify the gerbil’s sensitivity to amplitude modulation (AM) and carrier periodicity (CP) in broad-band stimuli. Two additional experiments investigate a possible interaction of the two types of periodicity. The results show that overall sensitivity to AM and CP is considerably less than in humans (by at least 10 dB). The gerbil’s amplitude-modulation sensitivity is almost independent of modulation frequency up to a modulation frequency of 1 kHz. Above, amplitude-modulation sensitivity deteriorates dramatically. On the basis of individual animals, carrier-periodicity detection may improve with increasing fundamental frequency up to about 500 Hz or may be independent of fundamental frequency. Amplitude-modulation thresholds are consistent with the hypothesis that intensity difference limens in the gerbil may be considerably worse than in humans, leading to the relative insensitivity for low modulation frequencies. Unlike in humans, inner-ear filtering appears not to limit amplitude-modulation sensitivity in the gerbil. Carrier-periodicity sensitivity changes with fundamental frequency similar to humans. Unlike in humans, there is no systematic interaction between AM and CP in the gerbil. This points to a relatively independent processing of the perceptual cues associated with AM and CP.     

Cigarette Smoking Causes Hearing Impairment among Bangladeshi Population

Lifestyle including smoking, noise exposure with MP3 player and drinking alcohol are considered as risk factors for affecting hearing synergistically. However, little is known about the association of cigarette smoking with hearing impairment among subjects who carry a lifestyle without using MP3 player and drinking alcohol. We showed here the influence of smoking on hearing among Bangladeshi subjects who maintain a lifestyle devoid of using MP3 player and drinking alcohol. A total of 184 subjects (smokers: 90; non-smokers: 94) were included considering their duration and frequency of smoking for conducting this study. The mean hearing thresholds of non-smoker subjects at 1, 4, 8 and 12 kHz frequencies were 5.63±2.10, 8.56±5.75, 21.06±11.06, 40.79±20.36 decibel (dB), respectively and that of the smokers were 7±3.8, 13.27±8.4, 30.66±12.50 and 56.88±21.58 dB, respectively. The hearing thresholds of the smokers at 4, 8 and 12 kHz frequencies were significantly (p<0.05) higher than those of the non-smokers, while no significant differences were observed at 1 kHz frequency. We also observed no significant difference in auditory thresholds among smoker subgroups based on smoking frequency. In contrast, subjects smoked for longer duration (>5 years) showed higher level of auditory threshold (62.16±19.87 dB) at 12 kHz frequency compared with that (41.52±19.21 dB) of the subjects smoked for 1-5 years and the difference in auditory thresholds was statistically significant (p<0.0002). In this study, the Brinkman Index (BI) of smokers was from 6 to 440 and the adjusted odds ratio showed a positive correlation between hearing loss and smoking when adjusted for age and body mass index (BMI). In addition, age, but not BMI, also played positive role on hearing impairment at all frequencies. Thus, these findings suggested that cigarette smoking affects hearing level at all the frequencies tested but most significantly at extra higher frequencies.     

Frequency sensitivity and directional hearing in the gleaning bat,Plecotus auritus (Linnaeus 1758)

1. The neural audiogram of the common long-eared bat, Plecotus auritus was recorded from the inferior colliculus (IC). The most sensitive best frequency (BF) thresholds for single neurones are below 0 dB SPL between 7-20 kHz, reaching a best value of -20 dB SPL between 12-20 kHz. The lower and upper limits of hearing occur at 3 kHz and 63 kHz, respectively, based on BF thresholds at 80 dB SPL. BF threshold sensitivities are about 10 dB SPL between 25-50 kHz, corresponding to the energy band of the sonar pulse (26-78 kHz). The tonotopic organization of the central nucleus of the IC (ICC) reveals that neurones with BFs below 20 kHz are disproportionately represented, occupying about 30% of ICC volume, occurring in the more rostral and lateral regions of the nucleus. 2. The acoustical gain of the external ear reaches a peak of about 20 dB between 8-20 kHz. The gain of the pinna increases rapidly above 4 kHz, to a peak of about 15 dB at 7-12 kHz. The pinna gain curve is similar to that of a simple, finite length acoustic horn; expected horn gain is calculated from the average dimensions of the pinna. 3. The directional properties of the external ear are based on sound diffraction by the pinna mouth, which, to a first approximation, is equivalent to an elliptical opening due to the elongated shape of the pinna. The spatial receptive field properties for IC neurones are related to the directional properties of the pinna. The position of the acoustic axis of the pinna and the best position (BP) of spatial receptive fields are both about 25 degrees from the midline between 8-30 kHz but approach the midline to 8 degrees at 45 kHz. In elevation, the acoustic axis and the BP of receptive fields move upwards by 20 degrees between 9-25 kHz, remaining stationary for frequencies up to 60 kHz. 4. The extremely high auditory sensitivity shown by the audiogram and the directionality of hearing are discussed in terms of the adaptation of the auditory system to low frequencies and the role of a large pinna in P. auritus. The functional significance of low frequency hearing in P. auritus is discussed in relation to hunting for prey by listening and is compared to other gleaning species.     

Directional hearing of a cicada: biophysical aspects

The directional hearing of male and female cicadas of the species Tympanistalna gastrica was investigated by means of laser vibrometry. The results show that the tympanic organs act as pressure difference receivers. This mechanism can produce left-right differences of more than 10 dB. The main acoustic inputs to the inner surfaces of the ears are the tympana, in males supplemented by the timbals, and by the third spiracles in females. In addition the hollow abdomen of males seems to play a minor role. Tympanic membrane input is the source of left-right differences in the tympanic vibration velocity at frequencies below 9 kHz in males and below 15–18 kHz in females. The input via the (contralateral) timbal in males is responsible for a null in vibration velocity appearing between 12 and 14 kHz when the sound is coming from the contralateral direction. The highest energy components of the calling song are found in this frequency range. The mechanical sensitivity of the ears depends upon the sex. At low frequencies males are about 10 dB more sensitive than females.     

Hearing of old world monkeys (Cercopithecinae)

The characteristics of normal hearing were examined in the laboratory for seven species of Old World monkeys. Operant conditioning procedures, coupled with standard audiometric testing methods, were used to assess thresholds of hearing, frequency range of hearing, and differential sensitivity to auditory intensity and frequency. To produce tonal stimulation, an animal was trained to touch and maintain manual contact with a contact-sensitive key and to report hearing the tone by lifting his hand from the key; this response was followed by food reinforcement. When the reporting response occurred without the auditory signal, the animal was punished by a short suspension from the experiment. Additional contingencies were added to ensure stable and reliable responding, and threshold and differential acuity determinations were then made. Threshold was defined as the stimulus value responded to correctly 50% of the time. The frequency range of hearing of all the cercopithecoids tested extended from 60 to 40,000 Hz, an octave above the upper bound of 20,000 Hz for man but well below the 60–70,000 Hz limit for some prosimians. Absolute sensitivity for tonal stimulation in the most sensitive frequency range (1–8 kHz) was about 2 × 10^?4 microbars, comparable to that of other primates tested, including man. Thus, the Old World monkey appears only slightly less sensitive than man to small changes in intensity and frequency of acoustic stimulation. At 1000 Hz at 60 dB above the threshold of audibility, his limit of resolution is about 5 Hz for frequency and 2 dB for intensity.     

Neural response to very low-frequency sound in the avian cochlear nucleus

Recordings were made in the chick cochlear nucleus from neurons that are sensitive to very low frequency sound. The tuning, discharge rate response and phase-locking properties of these units are described in detail. The principal conclusions are: 1. Low frequency (LF) units respond to sound frequencies between 10-800 Hz. Best thresholds average 60 dB SPL, and are occasionally as low as 40 dB SPL. While behavioral thresholds in this frequency range are not available for the domestic chick, these values are in good agreement with the pigeon behavioral audiogram (Kreithen and Quine 1979). 2. About 60% of the unit population displays tuning curves resembling low-pass filter functions with corner frequencies between 50-250 Hz. The remaining units have broad band-pass tuning curves. Best frequencies range from 50-300 Hz. 3. Spontaneous discharge rate was analyzed quantitatively for LF units recorded from nucleus angularis. The distribution of spontaneous rates for LF units is similar to that seen from higher CF units (300-5000 Hz) found in the same nucleus. However, the spontaneous firing of LF units is considerably more regular than that of their higher CF counterparts. 4. Low frequency units with low spontaneous rates (SR's less than 40 spikes/s) show large driven rate increases and usually saturate by discharging once or twice per stimulus cycle. Higher SR units often show no driven rate increases. 5. All LF units show strong phase-locking at all excitatory stimulus frequencies. Vector strengths as high as 0.98 have been observed at moderate sound levels. 6. The preferred phase of discharge (relative to the sound stimulus) increases with stimulus frequency in a nearly linear manner. This is consistent with the LF units being stimulated by a traveling wave. The slope of these phase-frequency relationships provides an estimate of traveling wave delay. These delays average 7.2 ms, longer than those seen for higher CF auditory brainstem units. These observations suggest that the peripheral site of low frequency sensitivity is the very distal region of the basilar papilla, an area whose morphology differs significantly from the rest of the chick basilar papilla. 7. LF units are described whose response to sound is inhibitory at frequencies above 50 Hz.     

Amplitude modulation thresholds for the parakeet (Melopsittacus undulatus)

Summary Parakeets were tested for the ability to detect sinusoidal amplitude modulation of broad band noise. Instrumental avoidance conditioning and a psychophysical modified method of limits procedure were used to measure the threshold for detecting amplitude modulation at 10 modulation frequencies between 2 and 2,048 Hz. Below about 40 Hz, modulation threshold is independent of modulation rate and noise level. Above 40 Hz, modulation threshold decreases with modulation frequency at the rate of 3 dB/ octave. These results are somewhat different from amplitude modulation functions in humans suggesting different degrees of temporal resolving power in birds and humans. Thresholds for changes in modulation rate are 1–2 orders of magnitude higher than pure tone frequency difference limens.We thank Frank Cusimano, Ann Huessener, Susan Peters, Roberta Pickert, Bill Searcy, Ken Yasukawa and Tim DeVoogd for participating as subjects, and Dick Fay for providing critical comments. This research was supported by grant No. PHS MH31165 from the National Institute of Mental Health to the first author.