Correspondence between evoked vocal responses and auditory thresholds in Pleurodema thaul (Amphibia; Leptodactylidae)

Thresholds for evoked vocal responses and thresholds of multiunit midbrain auditory responses to pure tones and synthetic calls were investigated in males of Pleurodema thaul, as behavioral thresholds well above auditory sensitivity have been reported for other anurans. Thresholds for evoked vocal responses to synthetic advertisement calls played back at increasing intensity averaged 43 dB RMS SPL (range 31–52 dB RMS SPL), measured at the subjects’ position. Number of pulses increased with stimulus intensities, reaching a plateau at about 18–39 dB above threshold and decreased at higher intensities. Latency to call followed inverse trends relative to number of pulses. Neural audiograms yielded an average best threshold in the high frequency range of 46.6 dB RMS SPL (range 41–51 dB RMS SPL) and a center frequency of 1.9 kHz (range 1.7–2.6 kHz). Auditory thresholds for a synthetic call having a carrier frequency of 2.1 kHz averaged 44 dB RMS SPL (range 39–47 dB RMS SPL). The similarity between thresholds for advertisement calling and auditory thresholds for the advertisement call indicates that male P. thaul use the full extent of their auditory sensitivity in acoustic interactions, likely an evolutionary adaptation allowing chorusing activity in low-density aggregations.     

What Do Primates Hear? A Meta-analysis of All Known Nonhuman Primate Behavioral Audiograms

Research on the hearing abilities of nonhuman primates dates back >70 yr and there are audiograms —graphs showing hearing sensitivity over a range of frequencies— for 29 different species including representatives from almost every major group. However, the methods used to obtain the audiograms have been nearly as varied as the number of species tested. I sought to determine the degree to which one can directly compare the audiograms by examining several factors that could have a significant impact on the results: the behavioral conditioning procedure employed to train and test the subjects, the type of transducer used to deliver the test tones, the procedure used to calibrate the amplitude of the test tones, the acoustic enclosure used to minimize ambient noise, and the method used to determine the final threshold values. Audiograms produced using speakers cannot be compared directly with those produced using headphones, and in some cases the calibration procedure and testing chamber may also limit the potential for interspecific comparisons. Based on the findings, I provide 2 lists of optimal primate audiograms: 1 for speaker-derived audiograms and the other for headphone-derived audiograms. I measured a set of audiometric variables on each of the optimal audiograms, and phylogenetic comparisons of the data show that superfamilies of primates display unique patterns of hearing sensitivity, particularly at frequencies in the lower range. Lastly, I discuss the implications for behavioralists investigating primate vocalizations in the field.     

A comparative study of hearing ability in fishes: the auditory brainstem response approach

Auditory brainstem response (ABR) techniques, an electrophysiological far-field recording method widely used in clinical evaluation of human hearing, were adapted for fishes to overcome the major limitations of traditional behavioral and electrophysiological methods (e.g., invasive surgery, lengthy training of fishes, etc.) used for fish hearing research. Responses to clicks and tone bursts of different frequencies and amplitudes were recorded with cutaneous electrodes. To evaluate the effectiveness of this method, the auditory sensitivity of a hearing specialist (goldfish, Carassius auratus) and a hearing generalist (oscar, Astronotus ocellatus) was investigated and compared to audiograms obtained through psychophysical methods. The ABRs could be obtained between 100 Hz and 2000 Hz (oscar), and up to 5000 Hz (goldfish). The ABR audiograms are similar to those obtained by behavioral methods in both species. The ABR audiogram of curarized (i.e., Flaxedil-treated) goldfish did not differ significantly from two previously published behavioral curves but was lower than that obtained from uncurarized fish. In the oscar, ABR audiometry resulted in lower thresholds and a larger bandwidth than observed in behavioral tests. Comparison between methods revealed the advantages of this technique: rapid evaluation of hearing in untrained fishes, and no limitations on repeated testing of animals. Accepted: 8 August 1997     

A test of the matched filter hypothesis in two sympatric frogs,Chiromantis doriae and Feihyla vittata

The matched filter hypothesis proposes that the auditory sensitivity of receivers should match the spectral energy distribution of the senders’ signals. If so, receivers should be able to distinguish between species-specific and hetero-specific signals. We tested the matched filter hypothesis in two sympatric species, Chiromantis doriae and Feihyla vittata, whose calls exhibit similar frequency characters and that overlap in the breeding season and microenvironment. For both species, we recorded male calls and measured the auditory sensitivity of both sexes using the auditory brainstem response (ABR). We compared the auditory sensitivity with the spectral energy distribution of the calls of each species and found that (1) auditory sensitivity matched the signal spectrogram in C. doriae and F. vittata; (2) the concordance conformed better to the conspecific signal versus the hetero-specific signal. In addition, our results show that species differences are larger than sex differences for ABR audiograms.     

Behaviorally measured audiograms and gap detection thresholds in CBA/CaJ mice

Tone detection and temporal gap detection thresholds were determined in CBA/CaJ mice using a Go/No-go procedure and the psychophysical method of constant stimuli. In the first experiment, audiograms were constructed for five CBA/CaJ mice. Thresholds were obtained for eight pure tones ranging in frequency from 1 to 42 kHz. Audiograms showed peak sensitivity between 8 and 24 kHz, with higher thresholds at lower and higher frequencies. In the second experiment, thresholds for gap detection in broadband and narrowband noise bursts were measured at several sensation levels. For broadband noise, gap thresholds were between 1 and 2 ms, except at very low sensation levels, where thresholds increased significantly. Gap thresholds also increased significantly for low pass-filtered noise bursts with a cutoff frequency below 18 kHz. Our experiments revised absolute auditory thresholds in the CBA/CaJ mouse strain and demonstrated excellent gap detection ability in the mouse. These results add to the baseline behavioral data from normal-hearing mice which have become increasingly important for assessing auditory abilities in genetically altered mice.     

Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals

The fish auditory system encodes important acoustic stimuli used in social communication, but few studies have examined response properties of central auditory neurons to natural signals. We determined the features and responses of single hindbrain and midbrain auditory neurons to tone bursts and playbacks of conspecific sounds in the soniferous damselfish, Abudefduf abdominalis. Most auditory neurons were either silent or had slow irregular resting discharge rates <20 spikes s⁻¹. Average best frequency for neurons to tone stimuli was ~130 Hz but ranged from 80 to 400 Hz with strong phase-locking. This low-frequency sensitivity matches the frequency band of natural sounds. Auditory neurons were also modulated by playbacks of conspecific sounds with thresholds similar to 100 Hz tones, but these thresholds were lower than that of tones at other test frequencies. Thresholds of neurons to natural sounds were lower in the midbrain than the hindbrain. This is the first study to compare response properties of auditory neurons to both simple tones and complex stimuli in the brain of a recently derived soniferous perciform that lacks accessory auditory structures. These data demonstrate that the auditory fish brain is most sensitive to the frequency and temporal components of natural pulsed sounds that provide important signals for conspecific communication.     

Evoked potentials of the auditory cortex of the porpoise,Phocoena phocoena

Summary Evoked potential (EP) recordings in the auditory cortex of the porpoise,Phocoena phocoena, were used to obtain data characterizing the auditory perception of this dolphin. The frequency threshold curves showed that the lowest EP thresholds were within 120–130 kHz. An additional sensitivity peak was observed between 20 and 30 kHz. The minimal EP threshold to noise burst was 3·10^–4–10^/s-3 Pa. The threshold for response to modulations in sound intensity was below 0.5 dB and about 0.1% for frequency modulations. Special attention was paid to the dependence of the auditory cortex EP on the temporal parameters of the acoustic stimuli: sound burst duration, rise time, and repetition rate. The data indicate that the porpoise auditory cortex is adapted to detect ultrasonic, brief, fast rising, and closely spaced sounds like echolocating clicks.Abbreviation EP evoked potential     

Evoked Potential Audiograms of the Nurse Shark (Ginglymostoma cirratum) and the Yellow Stingray (Urobatis jamaicensis)

The hearing thresholds of the nurse shark, Ginglymostoma cirratum, and the yellow stingray, Urobatis jamaicensis, were measured using auditory evoked potentials (AEP). Stimuli were calibrated using a pressure-velocity probe so that the acoustic field could be completely characterized. The results show similar hearing thresholds for both species and similar hearing thresholds to previously measured audiograms for the lemon shark, Negaprion brevirostris, and the horn shark, Heterodontis francisi. All of these audiograms suggest poor hearing abilities, raising questions about field studies showing attraction of sharks to acoustic signals. By extrapolating the particle acceleration thresholds into estimates of their equivalent far-field sound pressure levels, it appears that these sharks cannot likely detect most of the sounds that have attracted sharks in the field.     

Ontogeny of auditory saccular sensitivity in the plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The auditory system of the plainfin midshipman fish, Porichthys notatus, is an important sensory receiver system used to encode intraspecific social communication signals in adults, but the response properties and function of this receiver system in pre-adult stages are less known. In this study we examined the response properties of auditory-evoked potentials from the midshipman saccule, the main organ of hearing in this species, to determine whether the frequency response and auditory threshold of saccular hair cells to behaviorally relevant single tone stimuli change during ontogeny. Saccular potentials were recorded from three relative sizes of midshipman fish: small juveniles [1.9–3.1 cm standard length (SL), large juveniles (6.8–8.0 cm SL) and non-reproductive adults (9.0–22.6 cm SL)]. The auditory evoked potentials were recorded from the rostral, middle and caudal regions of the saccule while single tone stimuli (75–1,025 Hz) were presented via an underwater speaker. We show that the frequency response and auditory threshold of the midshipman saccule is established early in development and retained throughout ontogeny. We also show that saccular sensitivity to frequencies greater than 385 Hz increases with age/size and that the midshipman saccule of small and large juveniles, like that of non-reproductive adults, is best suited to detect low frequency sounds (<105 Hz) in their natural acoustic environment.     

Auditory sensitivity and ecological relevance: the functional audiogram as modelled by the bat detecting moth ear

Auditory sensitivity has often been measured by identifying neural threshold in real-time (online) which can introduce bias in the audiograms that are produced. We tested this by recording auditory nerve activity of the notodontid moth Nadata gibbosa elicited by bat-like ultrasound and analysing the response offline. We compared this audiogram with a published online audiogram showing that the bias introduced can result in a difference in the audiogram shape. In the second part of our study we compared offline audiograms using spike number as threshold with others that used spike period and stimulus/spike latency, variables that have been suggested as providing behaviourally functional criteria. These comparisons reveal that functional audiograms are more flatly tuned than simple spike audiograms. The shapes of behavioural audiograms are discussed in the context of the selection pressure that maintains their shape, bat predation. Finally, we make predictions on the distance from bats at which notodontid moths use negative phonotaxis or the acoustic startle response.     

Reduced acoustic startle response and peripheral hearing loss in the 5xFAD mouse model of Alzheimer's disease

Hearing dysfunction has been associated with Alzheimer's disease (AD) in humans, but there is little data on the auditory function of mouse models of AD. Furthermore, characterization of hearing ability in mouse models is needed to ensure that tests of cognition that use auditory stimuli are not confounded by hearing dysfunction. Therefore, we assessed acoustic startle response and pre‐pulse inhibition in the double transgenic 5xFAD mouse model of AD from 3–4 to 16 months of age. The 5xFAD mice showed an age‐related decline in acoustic startle as early as 3–4 months of age. We subsequently tested auditory brainstem response (ABR) thresholds at 4 and 13–14 months of age using tone bursts at frequencies of 2–32 kHz. The 5xFAD mice showed increased ABR thresholds for tone bursts between 8 and 32 kHz at 13–14 months of age. Finally, cochleae were extracted and basilar membranes were dissected to count hair cell loss across the cochlea. The 5xFAD mice showed significantly greater loss of both inner and outer hair cells at the apical and basal ends of the basilar membrane than wild‐type mice at 15–16 months of age. These results indicate that the 5xFAD mouse model of AD shows age‐related decreases in acoustic startle responses, which are at least partially due to age‐related peripheral hearing loss. Therefore, we caution against the use of cognitive tests that rely on audition in 5xFAD mice over 3–4 months of age, without first confirming that performance is not confounded by hearing dysfunction.     

Methods for determining auditory evoked brain-stem response thresholds in human newborns

Previous investigators have reported that newborn auditory evoked brain-stem responses (ABRs) are 20–30 dB higher than adult psychophysical thresholds to the same stimuli. These investigators reduced the intensity of the stimulus until they no longer reported an ABR to the stimulus. We adapted 2 widely used psychophysical methods, the up-down-transformed response (UDTR) method and the method of constant stimuli, for ABR threshold determination of human newborns. Response judgments were made blindly. ABR thresholds of healthy normal newborns by both procedures were no more than 10–15 dB higher than adult psychophysical thresholds. The differences between the newborn ABR thresholds we reported and those in the literature were probably explained by different procedures including the method used to estimate adult psychophysical thresholds. The correlations between ABR thresholds and suprathreshold ABR latencies and amplitudes and latency and amplitude/intensity functions were modest at best. In normal newborns suprathreshold ABR measurements are of little value in predicting ABR thresholds.     

Midbrain auditory sensitivity in the spring peeper (Pseudacris crucifer): correlations with behavioral studies

1. We derived audiograms from recordings of multiunit activity in the torus semicircularis of 10 males and 6 females of the spring peeper from central Missouri, USA. We used free-field stimulation with tone bursts that had temporal properties similar to typical advertisement calls and that ranged in frequency from 500-6000 Hz. 2. Audiograms from different electrode positions in the same animal had the same general shape. There was no evidence of tonotopy. 3. Audiograms showed two regions of maximal sensitivity: a low-frequency region (500-700 Hz); and a high-frequency region (2000-4000 Hz). Absolute thresholds and frequencies of maximum sensitivity varied considerably from individual to individual. 4. Audiograms derived from all individuals of each sex indicated that in the high-frequency region, corresponding to the frequency range of advertisement calls, males were more broadly tuned than females. However, tuning in both sexes was relatively weak, and the data predict relatively little selectivity in behavioral responses over the entire range of variation in frequency of the advertisement call in local populations. 5. The results are discussed in terms of behavioral experiments with both males and females from the same populations in central Missouri. We show that merely summarizing the audiograms based on estimates of minimum thresholds of a population or species may mask significant individual differences in tuning. Moreover, most behavioral studies are conducted at playback levels considerably above threshold. For these reasons, behavioral selectivity is not always accurately predicted by inspection of "average" audiograms.     

Evoked potential audiometry of 13 Pacific bottlenose dolphins (Tursiops truncatus gilli)

Evoked potential audiograms were measured in 13 Pacific bottlenose dolphins (Tursiops truncatus gilli) to determine the variability in hearing sensitivity and range of hearing. The auditory evoked potential system used a transducer embedded in a suction cup to deliver sinusoidal amplitude modulated tones to each dolphin through the pan region of the lower right jaw. Evoked potentials were recorded noninvasively using surface electrodes, and hearing thresholds were estimated by tracking the amplitude of the envelope following response, an evoked potential that is phase‐locked to the stimulus modulation rate. Frequencies tested ranged from 10 to 180 kHz in each animal. Variability in the range of hearing and age‐related reductions in hearing sensitivity and range of hearing were consistent with those observed in Atlantic bottlenose dolphins. Comparison of audiograms to a captive population of Atlantic bottlenose dolphins demonstrated that the Pacific bottlenose dolphins tested in this study had significantly lower thresholds at frequencies of 40 and 60–115 kHz. Differences in thresholds between the groups are unlikely to be due to methodological factors.     

Aerial hearing thresholds and detection of hearing loss in male California sea lions (Zalophus californianus) using auditory evoked potentials

Auditory evoked potential (AEP) measurements are useful for describing the variability of hearing among individuals in marine mammal populations, an important consideration in terms of basic biology and the design of noise mitigation criteria. In this study, hearing thresholds were measured for 16 male California sea lions at frequencies ranging from 0.5 to 32 kHz using the auditory steady state‐response (ASSR), a frequency‐specific AEP. Audiograms for most sea lions were grossly similar to previously reported psychophysical data in that hearing sensitivity increased with increasing frequency up to a steep reduction in sensitivity between 16 and 32 kHz. Average thresholds were not different from AEP thresholds previously reported for male and female California sea lions. Two sea lions from the current study exhibited abnormal audiograms: a 26‐yr‐old sea lion had impaired hearing with a high‐frequency hearing limit (HFHL) between 8 and 16 kHz, and an 8‐yr‐old sea lion displayed elevated thresholds across most tested frequencies. The auditory brainstem responses (ABRs) for these two individuals and an additional 26‐yr‐old sea lion were aberrant compared to those of other sea lions. Hearing loss may have fitness implications for sea lions that rely on sound during foraging and reproductive activities.     

Dissimilarities in auditory tuning in midwife toads of the genus Alytes (Amphibia: Anura)

The auditory sensitivity in three species of the anuran genus Alytes (Alytidae) was examined to determine patterns of intra‐ and interspecific variation, relating these measurements to behavioural preferences measured in previous studies and to the adaptive and evolutionary significance of this sensory function. The audiograms obtained with multi‐unit recordings in the torus semicircularis of 13 Alytes cisternasii, 10 Alytes obstetricans, and eight Alytes dickhilleni show two regions of enhanced sensitivity, between approximately 100–500 and 1200–2400 Hz, with minimum thresholds at approximately 40 and 45 dB SPL, respectively. The mean and range of the high‐frequency region differed among species, although the sensitivity, measured as minimum thresholds, was similar. The region of high‐frequency sensitivity was centred at approximately the frequency of the advertisement call in A. cisternasii but, in A. obstetricans and A. dickhilleni, was centred at frequencies higher than the conspecific calls. These results contrast with preferences for lower frequencies exhibited by Alytes in female phonotactic and in male evoked vocal responses. Such loose relationships between signals and receivers suggest that the divergence of the sound communication system in Alytes has implied environmental and phylogenetic factors in addition to sexual selection processes.     

Plasticity of Peripheral Auditory Frequency Sensitivity in Emei Music Frog

In anurans reproductive behavior is strongly seasonal. During the spring, frogs emerge from hibernation and males vocalize for mating or advertising territories. Female frogs have the ability to evaluate the quality of the males'' resources on the basis of these vocalizations. Although studies revealed that central single torus semicircularis neurons in frogs exhibit season plasticity, the plasticity of peripheral auditory sensitivity in frog is unknown. In this study the seasonally plasticity of peripheral auditory sensitivity was test in the Emei music frog Babina daunchina, by comparing thresholds and latencies of auditory brainstem responses (ABRs) evoked by tone pips and clicks in the reproductive and non-reproductive seasons. The results show that both ABR thresholds and latency differ significantly between the reproductive and non-reproductive seasons. The thresholds of tone pip evoked ABRs in the non-reproductive season increased significantly about 10 dB than those in the reproductive season for frequencies from 1 KHz to 6 KHz. ABR latencies to waveform valley values for tone pips for the same frequencies using appropriate threshold stimulus levels are longer than those in the reproductive season for frequencies from 1.5 to 6 KHz range, although from 0.2 to 1.5 KHz range it is shorter in the non-reproductive season. These results demonstrated that peripheral auditory frequency sensitivity exhibits seasonal plasticity changes which may be adaptive to seasonal reproductive behavior in frogs.     

Diminished behavioral and neural sensitivity to sound modulation is associated with moderate developmental hearing loss

The acoustic rearing environment can alter central auditory coding properties, yet altered neural coding is seldom linked with specific deficits to adult perceptual skills. To test whether developmental hearing loss resulted in comparable changes to perception and sensory coding, we examined behavioral and neural detection thresholds for sinusoidally amplitude modulated (sAM) stimuli. Behavioral sAM detection thresholds for slow (5 Hz) modulations were significantly worse for animals reared with bilateral conductive hearing loss (CHL), as compared to controls. This difference could not be attributed to hearing thresholds, proficiency at the task, or proxies for attention. Detection thresholds across the groups did not differ for fast (100 Hz) modulations, a result paralleling that seen in humans. Neural responses to sAM stimuli were recorded in single auditory cortex neurons from separate groups of awake animals. Neurometric analyses indicated equivalent thresholds for the most sensitive neurons, but a significantly poorer detection threshold for slow modulations across the population of CHL neurons as compared to controls. The magnitude of the neural deficit matched that of the behavioral differences, suggesting that a reduction of sensory information can account for limitations to perceptual skills.     

Auditory role of the suprabranchial chamber in gourami fish

Fish hearing specialists (e.g., goldfish, holocentrids, clupeoids, mormyrids) have evolved specialized structures (e.g., Weberian ossicles, swimbladder diverticulae, gas-filled bullae) to enhance their auditory frequency range and threshold sensitivity. The inner ears of anabantoid fish are encased in membranous cranial bones and are protruded into air-filled suprabranchial chambers. This research was intended to test the hypothesis that the gas bubbles inside the suprabranchial chambers may modulate the hearing abilities of anabantoid fish because of their proximity to the membranous bone-encased inner ears. Three species of gourami (blue gourami Trichogaster trichopterus; kissing gourami Helostoma temminckii; dwarf gourami Colisa lalia) were examined. Using the auditory brainstem response recording technique, baseline audiograms tested at 300, 500, 800, 1500, 2500, 4000 Hz were obtained. The air bubbles in the suprabranchial chambers were replaced by water, and the audiograms were remeasured. Thresholds were elevated in all three species. When three blue gouramis were allowed to replenish air into the suprabranchial chambers their hearing abilities returned to baseline levels. These results support the hypothesis that air bubbles in the suprabranchial chambers can affect hearing abilities of gouramis by lowering the thresholds. Accepted: 28 May 1998