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.     

Temporal resolution of the Risso’s dolphin, Grampus griseus, auditory system

Toothed whales and dolphins (Odontocetes) are known to echolocate, producing short, broadband clicks and receiving the corresponding echoes, at extremely rapid rates. Auditory evoked potentials (AEP) and broadband click stimuli were used to determine the modulation rate transfer function (MRTF) of a neonate Risso’s dolphin, Grampus griseus, thus estimating the dolphin’s temporal resolution, and quantifying its physiological delay to sound stimuli. The Risso’s dolphin followed sound stimuli up to 1,000 Hz with a second peak response at 500 Hz. A weighted MRTF reflected that the animal followed a broad range of rates from 100 to 1,000 Hz, but beyond 1,250 Hz the animal’s hearing response was simply an onset/offset response. Similar to other mammals, the dolphin’s AEP response to a single stimulus was a series of waves. The delay of the first wave, PI, was 2.76 ms and the duration of the multi-peaked response was 4.13 ms. The MRTF was similar in shape to other marine mammals except that the response delay was among the fastest measured. Results predicted that the Risso’s dolphin should have the ability to follow clicks and echoes while foraging at close range.     

Modulation rate transfer functions in bottlenose dolphins (<Emphasis Type="Italic">Tursiops truncatus</Emphasis>) with normal hearing and high-frequency hearing loss

Envelope following responses were measured in two bottlenose dolphins in response to sinusoidal amplitude modulated tones with carrier frequencies from 20 to 60 kHz and modulation rates from 100 to 5,000 Hz. One subject had elevated hearing thresholds at higher frequencies, with threshold differences between subjects varying from ±4 dB at 20 and 30 kHz to +40 dB at 50 and 60 kHz. At each carrier frequency, evoked response amplitudes and phase angles were plotted with respect to modulation frequency to construct modulation rate transfer functions. Results showed that both subjects could follow the stimulus envelope components up to at least 2,000 Hz, regardless of carrier frequency. There were no substantial differences in modulation rate transfer functions for the two subjects suggesting that reductions in hearing sensitivity did not result in reduced temporal processing ability. In contrast to earlier studies, phase data showed group delays of approximately 3.5 ms across the tested frequency range, implying generation site(s) within the brainstem rather than the periphery at modulation rates from 100 to 1,600 Hz. This discrepancy is believed to be the result of undersampling of the modulation rate during previous phase measurements.     

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.     

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.     

Detection of low‐frequency tones and whale predator sounds by the American sand lance Ammodytes americanus

Auditory evoked potentials (AEP) were used to measure the hearing range and auditory sensitivity of the American sand lance Ammodytes americanus. Responses to amplitude‐modulated tone pips indicated that the hearing range extended from 50 to 400 Hz. Sound pressure thresholds were lowest between 200 and 400 Hz. Particle acceleration thresholds showed an improved sensitivity notch at 200 Hz but not substantial differences between frequencies and only a slight improvement in hearing abilities at lower frequencies. The hearing range was similar to Pacific sand lance Ammodytes personatus and variations between species may be due to differences in threshold evaluation methods. AEPs were also recorded in response to pulsed sounds simulating humpback whale Megaptera novaeangliae foraging vocalizations termed megapclicks. Responses were generated with pulses containing significant energy below 400 Hz. No responses were recorded using pulses with peak energy above 400 Hz. These results show that A. americanus can detect the particle motion component of low‐frequency tones and pulse sounds, including those similar to the low‐frequency components of megapclicks. Ammodytes americanus hearing may be used to detect environmental cues and the pulsed signals of mysticete predators.     

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.     

Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics

In this study we recorded auditory brainstem responses to airborne sounds to determine the hearing sensitivity of Xenopus laevis frogs and correlated their hearing profiles with middle ear characteristics. In newly metamorphosed frogs (body mass 0.5–0.76 gm, snout-vent length 17–20 mm) best hearing sensitivities were measured in the 2.4–2.8 kHz range, whereas optimal hearing sensitivity of older adults (body mass 18–90 gm; snout-vent length 57–100 mm) ranged from 1.0 to 1.2 kHz. Middle ear volumes reconstructed from serial sections showed approximate volume of 0.002 cc and 0.04–0.07 cc in newly metamorphosed and older frogs, respectively. This inverse frequency–volume relationship is consistent with the properties of an acoustic resonator indicating that differences in best hearing sensitivity are at least in part correlated to variation in middle ear volumes for airborne sounds. These results are consistent with peak frequency vibrational velocity profiles of Xenopus tympanic disk that have been shown to be dependent on underlying middle ear volumes and corroborate the occurrence of peak amplitudes of otoacoustic emissions in the 1.0–1.2 kHz region in adult Xenopus frogs.     

Correlation between auditory sensitivity and vocalization in anabantoid fishes

Several anabantoid species produce broad-band sounds with high-pitched dominant frequencies (0.8–2.5 kHz), which contrast with generally low-frequency hearing abilities in (perciform) fishes. Utilizing a recently developed auditory brainstem response recording-technique, auditory sensitivities of the gouramis Trichopsis vittata, T. pumila, Colisa lalia, Macropodus opercularis and Trichogaster trichopterus were investigated and compared with the sound characteristics of the respective species. All five species exhibited enhanced sound-detecting abilities and perceived tone bursts up to 5 kHz, which qualifies this group as hearing specialists. All fishes possessed a high-frequency sensitivity maximum between 800 Hz and 1500 Hz. Lowest hearing thresholds were found in T. trichopterus (76 dB re 1 μPa at 800 Hz). Dominant frequencies of sounds correspond with the best hearing bandwidth in T. vittata (1–2 kHz) and C. lalia (0.8–1 kHz). In the smallest species, T. pumila, dominant frequencies of acoustic signals (1.5–2.5 kHz) do not match lowest thresholds, which were below 1.5 kHz. However, of all species studied, T. pumila had best hearing sensitivity at frequencies above 2 kHz. The association between high-pitched sounds and hearing may be caused by the suprabranchial air-breathing chamber, which, lying close to the hearing and sonic organs, enhances both sound perception and emission at its resonant frequency. Accepted: 26 November 1997     

Auditory temporal resolution of a wild white-beaked dolphin (<Emphasis Type="Italic">Lagenorhynchus albirostris</Emphasis>)

Adequate temporal resolution is required across taxa to properly utilize amplitude modulated acoustic signals. Among mammals, odontocete marine mammals are considered to have relatively high temporal resolution, which is a selective advantage when processing fast traveling underwater sound. However, multiple methods used to estimate auditory temporal resolution have left comparisons among odontocetes and other mammals somewhat vague. Here we present the estimated auditory temporal resolution of an adult male white-beaked dolphin, (Lagenorhynchus albirostris), using auditory evoked potentials and click stimuli. Ours is the first of such studies performed on a wild dolphin in a capture-and-release scenario. The white-beaked dolphin followed rhythmic clicks up to a rate of approximately 1,125–1,250 Hz, after which the modulation rate transfer function (MRTF) cut-off steeply. However, 10% of the maximum response was still found at 1,450 Hz indicating high temporal resolution. The MRTF was similar in shape and bandwidth to that of other odontocetes. The estimated maximal temporal resolution of white-beaked dolphins and other odontocetes was approximately twice that of pinnipeds and manatees, and more than ten-times faster than humans and gerbils. The exceptionally high temporal resolution abilities of odontocetes are likely due primarily to echolocation capabilities that require rapid processing of acoustic cues.     

Saccular potentials of the vocal plainfin midshipman fish, <Emphasis Type="Italic">Porichthys notatus</Emphasis>

The plainfin midshipman fish, Porichthys notatus, is a vocal species of teleost fish that generates acoustic signals for intraspecific communication during social and reproductive behaviors. All adult morphs (females and males) produce single short duration grunts important for agonistic encounters, but only nesting males produce trains of grunts and growls in agonistic contexts and long duration multiharmonic advertisement calls to attract gravid females for spawning. The midshipman fish uses the saccule as the main acoustic endorgan for hearing to detect and locate vocalizing conspecifics. Here, I examined the response properties of evoked potentials from the midshipman saccule to determine the frequency response and auditory threshold sensitivity of saccular hair cells to behaviorally-relevant single tone stimuli. Saccular potentials were recorded from the rostral, medial and caudal regions of the saccule while sound was presented by an underwater speaker. Saccular potentials of the midshipman, like other teleosts, were evoked greatest at a frequency that was twice the stimulus frequency. Results indicate that midshipman saccular hair cells of non-reproductive adults had a peak frequency sensitivity that ranged from 75 (lowest frequency tested) to 145 Hz and were best suited to detect the low frequency components (≤105 Hz) of midshipman vocalizations.     

Hearing loss in stranded odontocete dolphins and whales

The causes of dolphin and whale stranding can often be difficult to determine. Because toothed whales rely on echolocation for orientation and feeding, hearing deficits could lead to stranding. We report on the results of auditory evoked potential measurements from eight species of odontocete cetaceans that were found stranded or severely entangled in fishing gear during the period 2004 through 2009. Approximately 57% of the bottlenose dolphins and 36% of the rough-toothed dolphins had significant hearing deficits with a reduction in sensitivity equivalent to severe (70-90 dB) or profound (>90 dB) hearing loss in humans. The only stranded short-finned pilot whale examined had profound hearing loss. No impairments were detected in seven Risso's dolphins from three different stranding events, two pygmy killer whales, one Atlantic spotted dolphin, one spinner dolphin, or a juvenile Gervais' beaked whale. Hearing impairment could play a significant role in some cetacean stranding events, and the hearing of all cetaceans in rehabilitation should be tested.     

Auditory response characteristics of the piebald odorous frog and their implications

The piebald odorous frog (Odorrana schmackeri), the large odorous frog (Odorrana livida) and the concave-eared torrent frog (Amolops tormotus) are sympatric species living near the same torrent streams in the vicinity of Mt. Huangshan, China. A recent study demonstrated that A. tormotus can use sound signals involving ultrasonic components for communication in a noisy environment, and another sympatric species, O. livida, can also perceive ultrasonic sound. Here we report data on the hearing range of O. schmackeri by studying auditory evoked potentials and single-unit data from the torus semicircularis. This frog exhibits its two most sensitive peaks at 2 kHz and 3.5–4.0 kHz with thresholds <42 dB SPL, with an upper frequency limit of hearing at 8.5 kHz with threshold of 87 dB SPL. The upper limit is much lower than those of O. livida and A. tormotus, at 22 and 34 kHz, respectively. It suggests that sympatric species may respond differently to similar environmental selection pressures sculpting auditory communication systems.     

KILLER WHALE (ORCINUS ORCA) AUDITORY EVOKED POTENTIALS TO RHYTHMIC CLICKS

Temporal auditory mechanisms were measured in killer whales ( Orcinus orca ) by recording auditory evoked potentials (AEPs) to clicks. Clicks were presented at rates from 10/sec to 1,600/sec. At low rates, clicks evoked an AEP similar to the auditory brainstem response (ABR) of other odontocetes; however, peak latencies of the main waves were 3–3.7 msec longer than in bottlenose dolphins. Fourier analysis of the ABR showed a prominent peak at 300–400 Hz and a smaller one at 800–1,200 Hz. High-rate click presentation (more than 100/sec) evoked a rate-following response (RFR). The RFR amplitude depended little on rate up to 400/sec, decreased at higher rates and became undetectable at 1,120/sec. Fourier analysis showed that RFR fundamental amplitude dependence on frequency closely resembled the ABR spectrum. The fundamental could follow clicks to around 1,000/sec, although higher harmonics of lower rates could arise at frequencies as high as 1,200 Hz. Both RFR fundamental phase dependence on frequency and the response lag after a click train indicated an RFR group delay of around 7.5 msec. This corresponds to the latency of ABR waves PIII-NIV, which indicates the RFR originates as a rhythmic, overlapping ABR sequence. The data suggest the killer whale auditory system can follow high click rates, an ability that may have been selected for as a function of high-frequency hearing and the use of rapid clicks in echolocation.     

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     

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.     

Resonance phenomena in the cochlea of the mustache bat and their contribution to neuronal response characteristics in the cochlear nucleus

Summary The cochlea of the mustache bat, Pteronotus parnellii, is very sensitive and sharply tuned to the frequency range of the dominant second harmonic of the echolocation call around 61 kHz. About 900 Hz above this frequency the cochlear microphonic potential (CM) reaches its maximum amplitude and lowest threshold. At exactly the same frequency, pronounced evoked otoacoustic emissions (OAE) can be measured in the outer ear canal, indicating mechanical resonance. The CM amplitude maximum and the OAE are most severely masked by simultaneous exposure to tones within the range from about 61–62 kHz up to about 70 kHz. The data suggest that the mechanism of mechanical resonance involves cochlear loci basal to the 61 kHz position.The resonance contributes to auditory sensitivity and sharp tuning: At the frequency of the OAE, single unit responses in the cochlear nucleus have the lowest thresholds. Maximum tuning sharpness occurs at frequencies about 300 Hz below the OAE-frequency, where the threshold is about 10 dB less sensitive than at the OAE-frequency. In addition, in the frequency range around the OAE-frequency several specialized neuronal response features can be related to mechanical resonance: Long lasting excitation after the end of the stimulus, asymmetrical tuning curves with a shallow high frequency slope and phasic on-off neuronal response patterns. In particular the latter phenomenon indicates the occurrence of local mechanical cancellations in the cochlea.Abbreviations CF constant frequency component of echolocation calls - CM cochlear microphonic potential - FM frequency modulated component of echolocation calls - N1 compound action potential of the auditory nerve - OAE octoacoustic emission - SEOAE synchronous evoked OAE     

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     

Behavioral responses to jamming and ‘phantom’ jamming stimuli in the weakly electric fish <Emphasis Type="Italic">Eigenmannia</Emphasis>

The jamming avoidance response (JAR) of the weakly electric fish Eigenmannia is characterized by upward or downward shifts in electric organ discharge (EOD) frequency that are elicited by particular combinations of sinusoidal amplitude modulation (AM) and differential phase modulation (DPM). However, non-jamming stimuli that consist of AM and/or DPM can elicit similar shifts in EOD frequency. We tested the hypothesis that these behavioral responses result from non-jamming stimuli being misperceived as jamming stimuli. Responses to non-jamming stimuli were similar to JARs as measured by modulation rate tuning, sensitivity, and temporal dynamics. There was a smooth transition between the magnitude of JARs and responses to stimuli with variable depths of AM or DPM, suggesting that frequency shifts in response to jamming and non-jamming stimuli represent different points along a continuum rather than categorically distinct behaviors. We also tested the hypothesis that non-jamming stimuli can elicit frequency shifts in natural contexts. Frequency decreases could be elicited by semi-natural AM stimuli, such as random AM, AM presented to a localized portion of the body surface, transient changes in amplitude, and movement of resistive objects through the electric field. We conclude that ‘phantom’ jamming stimuli can induce EOD frequency shifts in natural situations.