Killer whale (Orcinus orca) hearing: auditory brainstem response and behavioral audiograms.

Killer whale (Orcinus orca) audiograms were measured using behavioral responses and auditory evoked potentials (AEPs) from two trained adult females. The mean auditory brainstem response (ABR) audiogram to tones between 1 and 100 kHz was 12 dB (re 1 mu Pa) less sensitive than behavioral audiograms from the same individuals (+/- 8 dB). The ABR and behavioral audiogram curves had shapes that were generally consistent and had the best threshold agreement (5 dB) in the most sensitive range 18-42 kHz, and the least (22 dB) at higher frequencies 60-100 kHz. The most sensitive frequency in the mean Orcinus audiogram was 20 kHz (36 dB), a frequency lower than many other odontocetes, but one that matches peak spectral energy reported for wild killer whale echolocation clicks. A previously reported audiogram of a male Orcinus had greatest sensitivity in this range (15 kHz, approximately 35 dB). Both whales reliably responded to 100-kHz tones (95 dB), and one whale to a 120-kHz tone, a variation from an earlier reported high-frequency limit of 32 kHz for a male Orcinus. Despite smaller amplitude ABRs than smaller delphinids, the results demonstrated that ABR audiometry can provide a useful suprathreshold estimate of hearing range in toothed whales.     

Measuring hearing in the harbor seal (Phoca vitulina): comparison of behavioral and auditory brainstem response techniques

Auditory brainstem response (ABR) and standard behavioral methods were compared by measuring in-air audiograms for an adult female harbor seal (Phoca vitulina). Behavioral audiograms were obtained using two techniques: the method of constant stimuli and the staircase method. Sensitivity was tested from 0.250 to 30 kHz. The seal showed good sensitivity from 6 to 12 kHz [best sensitivity 8.1 dB (re 20 microPa2 x s) RMS at 8 kHz]. The staircase method yielded thresholds that were lower by 10 dB on average than the method of constant stimuli. ABRs were recorded at 2, 4, 8, 16, and 22 kHz and showed a similar best range (8-16 kHz). ABR thresholds averaged 5.7 dB higher than behavioral thresholds at 2, 4, and 8 kHz. ABRs were at least 7 dB lower at 16 kHz, and approximately 3 dB higher at 22 kHz. The better sensitivity of ABRs at higher frequencies could have reflected differences in the seal's behavior during ABR testing and/or bandwidth characteristics of test stimuli. These results agree with comparisons of ABR and behavioral methods performed in other recent studies and indicate that ABR methods represent a good alternative for estimating hearing range and sensitivity in pinnipeds, particularly when time is a critical factor and animals are untrained.     

Behavioral and auditory evoked potential audiograms of a false killer whale (Pseudorca crassidens)

Behavioral and auditory evoked potential (AEP) audiograms of a false killer whale were measured using the same subject and experimental conditions. The objective was to compare and assess the correspondence of auditory thresholds collected by behavioral and electrophysiological techniques. Behavioral audiograms used 3-s pure-tone stimuli from 4 to 45 kHz, and were conducted with a go/no-go modified staircase procedure. AEP audiograms used 20-ms sinusoidally amplitude-modulated tone bursts from 4 to 45 kHz, and the electrophysiological responses were received through gold disc electrodes in rubber suction cups. The behavioral data were reliable and repeatable, with the region of best sensitivity between 16 and 24 kHz and peak sensitivity at 20 kHz. The AEP audiograms produced thresholds that were also consistent over time, with range of best sensitivity from 16 to 22.5 kHz and peak sensitivity at 22.5 kHz. Behavioral thresholds were always lower than AEP thresholds. However, AEP audiograms were completed in a shorter amount of time with minimum participation from the animal. These data indicated that behavioral and AEP techniques can be used successfully and interchangeably to measure cetacean hearing sensitivity.     

Auditory lateralization in monkeys: an examination of two cues serving directional hearing.

In assigning binaural ongoing time differences (phase) as the cue for localization of low frequencies, and binaural intensity differences as the cue for localization of high frequencies, the duplex theory has successfully accounted for human directional hearing of tones. Sensitivity of monkeys to these cues was examined in two experiments. The dependencies on frequency of interaural intensity difference thresholds (lateralization experiment I) and time difference thresholds (lateralization experiment II) were determined behaviorally on three monkeys (M. nemestrina). The range of frequencies was from 125 Hz to 8 kHz in experiment I and from 250 Hz to 2 kHz in experiment II. The results indicate that the duplex theory is applicable to monkeys. However, monkeys are less sensitive than man to both binaural cues. The shortest time disparity monkeys discriminate is 42 microseconds at 1.5 kHz and the smallest intensity difference is 3.5 dB at 500 Hz. Good agreement between the present findings and localization measurements [C. H. Brown et al., J. Acoust. Soc. Am. 63, 1484-1492 (1978)] suggests: (a) that monkeys utilize time disparity cues through higher frequencies than man; and (b) that inaccurate localization by monkeys at high frequencies reflects decreasing sensitivity to interaural intensity cues.     

Temporary threshold shift in bottlenose dolphins (Tursiops truncatus) exposed to mid-frequency tones

A behavioral response paradigm was used to measure hearing thresholds in bottlenose dolphins before and after exposure to 3 kHz tones with sound exposure levels (SELs) from 100 to 203 dB re 1 microPa2 s. Experiments were conducted in a relatively quiet pool with ambient noise levels below 55 dB re 1 microPa2/Hz at frequencies above 1 kHz. Experiments 1 and 2 featured 1-s exposures with hearing tested at 4.5 and 3 kHz, respectively. Experiment 3 featured 2-, 4-, and 8-s exposures with hearing tested at 4.5 kHz. For experiment 2, there were no significant differences between control and exposure sessions. For experiments 1 and 3, exposures with SEL=197 dB re 1 microPa2 s and SEL > or = 195 dB re 1 microPa2 s, respectively, resulted in significantly higher TTS4 than control sessions. For experiment 3 at SEL= 195 dB re 1 microPa2 s, the mean TTS4 was 2.8 dB. These data are consistent with prior studies of TTS in dolphins exposed to pure tones and octave band noise and suggest that a SEL of 195 dB re 1 microPa2 s is a reasonable threshold for the onset of TTS in dolphins and white whales exposed to midfrequency tones.     

Underwater audiogram of a false killer whale (Pseudorca crassidens)

Underwater audiograms are available for only a few odontocete species. A false killer whale (Pseudorca crassidens) was trained at Sea Life Park in Oahu, Hawaii for an underwater hearing test using a go/no-go response paradigm. Over a 6-month period, auditory thresholds from 2-115 kHz were measured using an up/down staircase psychometric technique. The resulting audiogram showed hearing sensitivities below 64 kHz similar to those of belugas (Delphinapterus leucas) and Atlantic bottlenosed dolphins (Tursiops truncatus). Above 64 kHz, this Pseudorca had a rapid decrease in sensitivity of about 150 dB per octave. A similar decrease in sensitivity occurs at 32 kHz in the killer whale, at 50 kHz in the Amazon River dolphin, at 120 kHz in the beluga, at 140 kHz in the bottlenosed dolphin, and at 140 kHz in the harbor porpoise. The most sensitive range of hearing was from 16-64 kHz (a range of 10 dB from the maximum sensitivity). This range corresponds with the peak frequency of echolocation pulses recorded from captive Pseudorca.     

Audiogram of a harbor porpoise (Phocoena phocoena) measured with narrow-band frequency-modulated signals

The underwater hearing sensitivity of a two-year-old harbor porpoise was measured in a pool using standard psycho-acoustic techniques. The go/no-go response paradigm and up-down staircase psychometric method were used. Auditory sensitivity was measured by using narrow-band frequency-modulated signals having center frequencies between 250 Hz and 180 kHz. The resulting audiogram was U-shaped with the range of best hearing (defined as 10 dB within maximum sensitivity) from 16 to 140 kHz, with a reduced sensitivity around 64 kHz. Maximum sensitivity (about 33 dB re 1 microPa) occurred between 100 and 140 kHz. This maximum sensitivity range corresponds with the peak frequency of echolocation pulses produced by harbor porpoises (120-130 kHz). Sensitivity falls about 10 dB per octave below 16 kHz and falls off sharply above 140 kHz (260 dB per octave). Compared to a previous audiogram of this species (Andersen, 1970), the present audiogram shows less sensitive hearing between 2 and 8 kHz and more sensitive hearing between 16 and 180 kHz. This harbor porpoise has the highest upper-frequency limit of all odontocetes investigated. The time it took for the porpoise to move its head 22 cm after the signal onset (movement time) was also measured. It increased from about 1 s at 10 dB above threshold, to about 1.5 s at threshold.     

Examination of bone-conducted transmission from sound field excitation measured by thresholds, ear-canal sound pressure, and skull vibrations

Bone conduction (BC) relative to air conduction (AC) sound field sensitivity is here defined as the perceived difference between a sound field transmitted to the ear by BC and by AC. Previous investigations of BC-AC sound field sensitivity have used different estimation methods and report estimates that vary by up to 20 dB at some frequencies. In this study, the BC-AC sound field sensitivity was investigated by hearing threshold shifts, ear canal sound pressure measurements, and skull bone vibrations measured with an accelerometer. The vibration measurement produced valid estimates at 400 Hz and below, the threshold shifts produced valid estimates at 500 Hz and above, while the ear canal sound pressure measurements were found erroneous for estimating the BC-AC sound field sensitivity. The BC-AC sound field sensitivity is proposed, by combining the present result with others, as frequency independent at 50 to 60 dB at frequencies up to 900 Hz. At higher frequencies, it is frequency dependent with minima of 40 to 50 dB at 2 and 8 kHz, and a maximum of 50 to 60 dB at 4 kHz. The BC-AC sound field sensitivity is the theoretical limit of maximum attenuation achievable with ordinary hearing protection devices.     

Pure tone audiograms and possible aminoglycoside-induced hearing loss in belugas (Delphinapterus leucas)

A behavioral response paradigm was used to measure pure-tone hearing sensitivities in two belugas (Delphinapterus leucas). Tests were conducted over a 20-month period at the Point Defiance Zoo and Aquarium, in Tacoma, WA. Subjects were two males, aged 8-10 and 9-11 during the course of the study. Subjects were born in an oceanarium and had been housed together for all of their lives. Hearing thresholds were measured using a modified up/down staircase procedure and acoustic response paradigm where subjects were trained to produce audible responses to test tones and to remain quiet otherwise. Test frequencies ranged from approximately 2 to 130 kHz. Best sensitivities ranged from approximately 40 to 50 dB re 1 microPa at 50-80 kHz and 30-35 kHz for the two subjects. Although both subjects possessed traditional "U-shaped" mammalian audiograms, one subject exhibited significant high-frequency hearing loss above 37 kHz compared to previously published data for belugas. Hearing loss in this subject was estimated to approach 90 dB for frequencies above 50 kHz. Similar ages, ancestry, and environmental conditions between subjects, but a history of ototoxic drug administration in only one subject, suggest that the observed hearing loss was a result of the aminoglycoside antibiotic amikacin.     

Auditory thresholds in a sound-producing electric fish (Pollimyrus): behavioral measurements of sensitivity to tones and click trains

In this report we present the first behavioral measurements of auditory sensitivity for Pollimyrus adspersus. Pollimyrus is an electric fish (Mormyridae) that uses both electric and acoustic signals for communication. Tone detection was assessed from the fish's electric organ discharge rate. Suprathreshold tones usually evoked an accelerated rate in naive animals. This response (rate modulation > or =25%) was maintained in a classical conditioning paradigm by presenting a weak electric current near the offset of 3.5-s tone bursts. An adaptive staircase procedure was used to find detection thresholds at frequencies between 100 and 1700 Hz. The mean audiogram from six individuals revealed high sensitivity in the 200-900 Hz range, with the best thresholds near 500 Hz (66.5+/-4.2 SE dB re: 1 microPa). Sensitivity declined slowly (about 20 dB/octave) above and below this sensitivity maximum. Sensitivity fell off rapidly above 1 kHz (about 60 dB/octave) and no responses were observed at 5 kHz. This behavioral sensitivity matched closely the spectral content of the sounds that this species produced during courtship. Experiments with click trains showed that sensitivity (about 83-dB peak) was independent of inter-click-interval, within the 10-100 ms range.     

Hearing sensitivity and critical ratios of hooded crows (Corvus corone cornix)

The hearing threshold and critical ratios were estimated psycho-acoustically for captive wild-caught hooded crows by a yes/no procedure and the method of constant stimuli. Human subjects were tested in the same setup for direct comparison and to check for experimental artifacts. The hooded crows were found to have excellent low-frequency hearing capabilities compared to other passerine birds. Their hearing sensitivity is very close to that of humans at and below 5.6 kHz. The distribution of the critical ratios differed from that of the average bird and humans in being rather constant with frequency and not increasing monotonically. It furthermore showed a middle region of 5-6 dB lower critical ratio values between 500 Hz and 2 kHz. It is suggested that this improved range for hearing in noise is an adaptation to long distance communication. Human critical ratios gave the expected values and were between 3 and 6 dB lower than those of the crows.     

Noise level, inner hair cell damage, audiometric features, and equal-energy hypothesis

Rabbits were exposed to 2- to 7-kHz noise either for a short duration at a high sound-pressure level (15 or 30 min at 115 dB SPL), or a long duration at a low level (512 h at 85 dB SPL). The high-level exposure produced a hearing loss in the frequency range 2-6 kHz, whereas the low-level exposure gave maximum hearing loss at 12-20 kHz. The 115-dB exposure caused significantly more damage to inner hair cells than the 85-dB exposure. The implications of the present results for evaluating audiograms, equal-energy hypothesis, risk criteria, and subjective auditory features are pointed out.     

Lateralization of acoustic signals by dichotically listening budgerigars (Melopsittacus undulatus)

Sound localization allows humans and animals to determine the direction of objects to seek or avoid and indicates the appropriate position to direct visual attention. Interaural time differences (ITDs) and interaural level differences (ILDs) are two primary cues that humans use to localize or lateralize sound sources. There is limited information about behavioral cue sensitivity in animals, especially animals with poor sound localization acuity and small heads, like budgerigars. ITD and ILD thresholds were measured behaviorally in dichotically listening budgerigars equipped with headphones in an identification task. Budgerigars were less sensitive than humans and cats, and more similar to rabbits, barn owls, and monkeys, in their abilities to lateralize dichotic signals. Threshold ITDs were relatively constant for pure tones below 4 kHz, and were immeasurable at higher frequencies. Threshold ILDs were relatively constant over a wide range of frequencies, similar to humans. Thresholds in both experiments were best for broadband noise stimuli. These lateralization results are generally consistent with the free field localization abilities of these birds, and add support to the idea that budgerigars may be able to enhance their cues to directional hearing (e.g., via connected interaural pathways) beyond what would be expected based on head size.     

The underwater audiogram of the West Indian manatee (Trichechus manatus).

The hearing thresholds of two adult manatees were measured using a forced-choice two alternative paradigm and an up/down staircase psychometric method. This is the first behavioral audiogram measured for any Sirenian, as well as the first underwater infrasonic psychometric test with a marine mammal. Auditory thresholds were obtained from 0.4 to 46 kHz, and detection thresholds of possible vibrotactile origin were measured at 0.015-0.2 kHz. The U-shaped audiogram demonstrates an upper limit of functional hearing at 46 kHz with peak frequency sensitivity at 16 and 18 kHz (50 dB re: 1 microPa). The range of best hearing is 6-20 kHz (approximately 9 dB down from maximum sensitivity). Sensitivity falls 20 dB per octave below 0.8 kHz and approximately 40 dB per octave above 26 kHz. The audiogram demonstrates a wider range of hearing and greater sensitivity than was suggested from evoked potential and anatomical studies. High frequency sensitivity may be an adaptation to shallow water, where the propagation of low frequency sound is limited by physical boundary effects. Hearing abilities of manatees and other marine mammals may have also been shaped by ambient and thermal noise curves in the sea. Inadequate hearing sensitivity at low frequencies may be a contributing factor to the manatees' inability to effectively detect boat noise and avoid collisions with boats.     

Resolution in azimuth sound localization in the Mongolian gerbil (Meriones unguiculatus)

Minimum resolvable angles (MRAs) for sound localization in azimuth in the gerbil were determined in a behavioral study using tones, 300-Hz bands of noise centered at frequencies between 500 Hz and 8 kHz and broad-band noise of on average 60 dB SPL overall level. Using the method of constant stimuli, seven gerbils were trained in a two-alternative-forced-choice procedure to indicate if sounds were presented to them from the left or from the right by choosing the left or right arm of a Y-shaped cage. The MRA is the minimum angle between two loudspeaker locations that the gerbils discriminated. Animals were either stimulated from the front (N=4) or from the back (N=3). The MRA for broad-band noise randomly varying in level by +/- 6 dB was 23 degrees and 45 degrees for gerbils stimulated from the front or back, respectively. Generally a gerbil's MRA for tones declined up to 2 kHz reaching 20 degrees and 31 degrees for gerbils stimulated from the front or back, respectively, and the MRA was generally increased above this frequency. Results for narrow-band noise stimuli were similar. Results are discussed with respect to the available interaural cues and physiological mechanisms of sound localization in the gerbil.     

A comparison of steady-state evoked potentials to modulated tones in awake and sleeping humans.

Steady-state evoked potential responses were measured to binaural amplitude-modulated (AM) and combined amplitude- and frequency-modulated (AM/FM) tones. For awake subjects, AM/FM tones produced larger amplitude responses than did AM tones. Awake and sleeping responses to 30-dB HL AM/FM tones were compared. Response amplitudes were lower during sleep and the extent to which they differed from awake amplitudes was dependent on both carrier and modulation frequencies. Background EEG noise at the stimulus modulation frequency was also reduced during sleep and varied with modulation frequency. A detection efficiency function was used to indicate the modulation frequencies likely to be most suitable for electrical estimation of behavioral threshold. In awake subjects, for all carrier frequencies tested, detection efficiency was highest at a modulation frequency of 45 Hz. In sleeping subjects, the modulation frequency regions of highest efficiency varied with carrier frequency. For carrier frequencies of 250 Hz, 500 Hz, and 1 kHz, the highest efficiencies were found in two modulation frequency regions centered on 45 and 90 Hz. For 2 and 4 kHz, the highest efficiencies were at modulation frequencies above 70 Hz. Sleep stage affected both response amplitude and background EEG noise in a manner that depended on modulation frequency. The results of this study suggest that, for sleeping subjects, modulation frequencies above 70 Hz may be best when using steady-state potentials for hearing threshold estimation.     

Toneburst-evoked auditory brainstem response in a leopard seal, Hydrurga leptonyx

Toneburst-evoked auditory brainstem responses (ABRs) were recorded in a captive subadult male leopard seal. Three frequencies from 1 to 4 kHz were tested at sound levels from 68 to 122 dB peak equivalent sound pressure level (peSPL). Results illustrate brainstem activity within the 1-4 kHz range, with better hearing sensitivity at 4 kHz. As is seen in human ABR, only wave V is reliably identified at the lower stimulus intensities. Wave V is present down to levels of 82 dB peSPL in the right ear and 92 dB peSPL in the left ear at 4 kHz. Further investigations testing a wider frequency range on seals of various sex and age classes are required to conclusively report on the hearing range and sensitivity in this species.     

Frequency and intensity discrimination in humans and monkeys

Frequency and intensity DLs were compared in humans and monkeys using a repeating standard "yes-no" procedure in which subjects reported frequency increments, frequency decrements, intensity increments, or intensity decrements in an ongoing train of 1.0-kHz tone bursts. There was only one experimental condition (intensity increments) in which monkey DLs (1.5-2.0 dB) overlapped those of humans (1.0-1.8 dB). For discrimination of both increments and decrements in frequency, monkey DLs (16-33 Hz) were approximately seven times larger than those of humans (2.4-4.8 Hz), and for discrimination of intensity decrements, monkey DLs (4.4-7.0 dB) were very unstable and larger than those of humans (1.0-1.8 dB). For intensity increment discrimination, humans and monkeys also exhibited similar DLs as SL was varied. However, for frequency increment discrimination, best DLs for humans occurred at a high (50 dB) SL, whereas best DLs for monkeys occurred at a moderate (30 dB) SL. Results are discussed in terms of various neural mechanisms that might be differentially engaged by humans and monkeys in performing these tasks; for example, different amounts of temporal versus rate coding in frequency discrimination, and different mechanisms for monitoring rate decreases in intensity discrimination. The implications of these data for using monkeys as models of human speech sound discrimination are also discussed.     

Psychometric functions for discrimination of two-component complex tones in listeners with normal hearing and listeners with hearing loss

This study compared the ability of 5 listeners with normal hearing and 12 listeners with moderate to moderately severe sensorineural hearing loss to discriminate complementary two-component complex tones (TCCTs). The TCCTs consist of two pure tone components (f1 and f2) which differ in frequency by delta f (Hz) and in level by delta L (dB). In one of the complementary tones, the level of the component f1 is greater than the level of component f2 by the increment delta L; in the other tone, the level of component f2 exceeds that of component f1 by delta L. Five stimulus conditions were included in this study: fc = 1000 Hz, delta L = 3 dB; fc = 1000 Hz, delta L = 1 dB; fc = 2000 Hz, delta L = 3 dB; fc = 2000 Hz, delta L = 1 dB; and fc = 4000 Hz, delta L = 3 dB. In listeners with normal hearing, discrimination of complementary TCCTs (with a fixed delta L and a variable delta f) is described by an inverted U-shaped psychometric function in which discrimination improves as delta f increases, is (nearly) perfect for a range of delta f's, and then decreases again as delta f increases. In contrast, group psychometric functions for listeners with hearing loss are shifted to the right such that above chance performance occurs at larger values of delta f than in listeners with normal hearing. Group psychometric functions for listeners with hearing loss do not show a decrease in performance at the largest values of delta f included in this study. Decreased TCCT discrimination is evident when listeners with hearing loss are compared to listeners with normal hearing at both equal SPLs and at equal sensation levels. In both groups of listeners, TCCT discrimination is significantly worse at high center frequencies. Results from normal-hearing listeners are generally consistent with a temporal model of TCCT discrimination. Listeners with hearing loss may have deficits in using phase locking in the TCCT discrimination task and so may rely more on place cues in TCCT discrimination.     

Speech reception in quiet and in noisy conditions by individuals with noise-induced hearing loss in relation to their tone audiogram.

Tone thresholds and speech-reception thresholds were measured in 200 individuals (400 ears) with noise-induced hearing loss. The speech-reception thresholds were measured in a quiet condition and in noise with a speech spectrum at levels of 35, 50, 65, and 80 dBA. The tone audiograms could be described by three principal components: hearing loss in the regions above 3 kHz, from 1 to 3 kHz and below 1 kHz; the speech thresholds could be described by two components: speech reception in quiet and speech reception in noise at 50-80 dBA. Hearing loss above 1 kHz was related to speech reception in noise; hearing loss at and below 1 kHz to speech reception in quiet. The correlation between the speech thresholds in quiet and in noise was only R = 0.45. An adequate predictor of the speech threshold in noise, the primary factor in the hearing handicap, was the pure-tone average at 2 and 4 kHz (PTA2,4, R = 0.72). The minimum value of the prediction error for any tone-audiometric predictor of this speech threshold was 1.2 dB (standard deviation). The prediction could not be improved by taking into account the critical ratio for low-frequency noise nor by its upward spread of masking. The prediction error is due to measurement error and to a factor common to both ears. The latter factor is ascribed to cognitive skill in speech reception. Hearing loss above 10 to 15 dB HL (hearing level) already shows an effect on the speech threshold in noise, a noticeable handicap is found at PTA2,4 = 30 dB HL.