Hearing in helmeted guineafowl (Numida meleagris): audiogram from 2 Hz to 10 kHz and localization acuity for brief noise bursts.

Behavioral hearing thresholds and noise localization acuity were determined using a conditioned avoidance/suppression procedure for three Helmeted guineafowl (Numida meleagris). The guineafowl responded to frequencies as low as 2 Hz at 82.5 dB SPL, and as high as 8 kHz at 84.5 dB SPL. At a level of 60 dB SPL, their hearing range spanned 8.12 octaves (24.6 Hz-6.86 kHz). Like most birds, they do not hear sounds above 8 kHz. However, the guineafowl demonstrated good low-frequency hearing (frequencies below 32 Hz), showing thresholds that are more sensitive than both the peafowl and pigeon, both of which hear infrasound. It thus appears that infrasound perception may be more common than previously thought and may have implications for species that inhabit areas with wind energy facilities. The guineafowls' minimum audible angle for a 100-ms broadband noise burst was 13.8 °, at the median for birds and near the mean for mammals. Unlike in mammals, the small sample of bird species and limited representation of lifestyles do not yet allow for meaningful interpretations of the selective pressures or mechanisms that underlie their abilities to locate sound sources.

Hearing in African pygmy hedgehogs (Atelerix albiventris): audiogram, sound localization, and ear anatomy.

The behavioral audiogram and sound localization performance, together with the middle and inner ear anatomy, were examined in African pygmy hedgehogs Atelerix albiventris. Their auditory sensitivity at 60 dB SPL extended from 2 to 46 kHz, revealing a relatively narrow hearing range of 4.6 octaves, with a best sensitivity of 21 dB at 8 kHz. Their noise-localization acuity around the midline (minimum audible angle) was 14°, matching the mean of terrestrial mammals. The African pygmy hedgehog was not able to localize low-frequency pure tones or a 3-kHz amplitude-modulated tone when forced to rely on the interaural phase-difference cue, a trait shared by at least nine other mammals. The middle ear of Atelerix has a configuration including an ectotympanic which is not fused to the surrounding bones, a substantial pars flaccida, a synostosed malleo-ectotympanic articulation and a 'microtype' malleus. The hearing and sound localization of A. albiventris is compared to that of a broad range of other mammals. It is shown that a malleus morphology like that of Atelerix, including a stiff articulation with the ectotympanic, is a consistent feature of other mammals that do not hear frequencies below 400 Hz.

Hearing and sound localization in Cottontail rabbits, Sylvilagus floridanus.

Cottontail rabbits represent the first wild species of the order of lagomorphs whose hearing abilities have been determined. Cottontails, Sylvilagus floridanus, evolved in the New World, but have spread worldwide. Their hearing was tested behaviorally using a conditioned-avoidance procedure. At a level of 60 dB SPL, their hearing ranged from 300 Hz to 32 kHz, a span of 7.5 octaves. Mammalian low-frequency hearing is bimodally distributed and Cottontail rabbits fall into the group that hears below 400 Hz. However, their 300-Hz limit puts them near the gap that separates the two populations. The minimum audible angle of cottontails is 27.6°, making them less acute than most other species of mammals. Their large sound-localization threshold is consistent with the observation that mammals with broad fields of best vision require less acuity to direct their eyes to the sources of sound.

Bats are unusually insensitive to brief low-frequency tones.

Bats use brief calls for echolocation, suggesting that they might be more sensitive to brief sounds than non-echolocating mammals. To investigate this possibility, absolute thresholds for brief tones were determined for four species of bats: The Common vampire bat (Desmodus rotundus) and the Greater spear-nosed bat (Phyllostomus hastatus), both of which use frequency-modulated calls, the Egyptian fruit bat (Rousettus aegyptiacus), an echolocator that uses tongue-clicks rather than laryngeal calls, and the Dog-faced fruit bat (Cynopterus brachyotis), a non-echolocating species. Norway rats and a human were tested for comparison using the same acoustic stimuli. Contrary to expectations, the echolocating bats were not superior to non-echolocating mammals in detecting brief tones in the frequency range of their echolocation calls. Instead, all four species of bats were remarkably less sensitive than non-bats to brief sounds of 10 kHz and below. This implies that temporal summation in the mammalian auditory system can show large species differences, and that the detection of brief sound is likely influenced by the selective pressures on each species as well as by the physical integration of energy in the auditory system. Such species differences in function are expected to be reflected in the physiology of their auditory systems.

Normal audiogram but poor sensitivity to brief sounds in mice with compromised voltage-gated sodium channels (Scn8amedJ).

The Scn8amedJ mutation of the gene for sodium channels at the nodes of Ranvier slows nerve conduction, resulting in motor abnormalities. This mutation is also associated with loss of spontaneous bursting activity in the dorsal cochlear nucleus. However initial tests of auditory sensitivity in mice homozygous for this mutation, using standard 400-ms tones, demonstrated normal hearing sensitivity. Further testing, reported here, revealed a severely compromised sensitivity to short-duration tones of 10 and 2 ms durations. Such a deficit might be expected to interfere with auditory functions that depend on rapid processing of auditory signals.

Comments on "Killer whale (Orcinus orca) behavioral audiograms" [J. Acoust. Soc. Am. 141, 2387-2398 (2017)].

Branstetter and his colleagues present the audiograms of eight killer whales and provide a comprehensive review of previous killer whale audiograms. In their paper, they say that the present authors have reported a relationship between size and high-frequency hearing but that echolocating cetaceans might be a special case. The purpose of these comments is to clarify that the relationship of a species' high-frequency hearing is not to its size (mass) but to its "functional interaural distance" (a measure of the availability of sound-localization cues). Moreover, it has previously been noted that echolocating animals, cetaceans as well as bats, have extended their high-frequency hearing somewhat beyond the frequencies used by comparable non-echolocators for passive localization.

Budgerigars (Melopsittacus undulatus) do not hear infrasound: the audiogram from 8 Hz to 10 kHz.

The pure-tone thresholds of three budgerigars were determined from 8 Hz to 10 kHz. At a level of 60 dB sound pressure level (re 20 µN/m2), their hearing range extends 6.6 octaves from 77 Hz to 7.6 kHz, with a best sensitivity of 1.1 dB at 3 kHz. Unlike pigeons and chickens, budgerigars do not have better low-frequency hearing than humans. This difference implies anatomical, physiological, and ecological differences between birds that hear infrasound (so far, pigeons and chickens) and those that do not (budgerigars).

Volumes of cochlear nucleus regions in rodents.

The cochlear nucleus receives all the coded information about sound from the cochlea and is the source of auditory information for the rest of the central auditory system. As such, it is a critical auditory nucleus. The sizes of the cochlear nucleus as a whole and its three major subdivisions - anteroventral cochlear nucleus (AVCN), posteroventral cochlear nucleus (PVCN), and dorsal cochlear nucleus (DCN) - have been measured in a large number of mammals, but measurements of its subregions at a more detailed level for a variety of species have not previously been made. Size measurements are reported here for the summed granular regions, DCN layers, AVCN, PVCN, and interstitial nucleus in 15 different rodent species, as well as a lagomorph, carnivore, and small primate. This further refinement of measurements is important because the granular regions and superficial layers of the DCN appear to have some different functions than the other cochlear nucleus regions. Except for DCN layers in the mountain beaver, all regions were clearly identifiable in all the animals studied. Relative regional size differences among most of the rodents, and even the 3 non-rodents, were not large and did not show a consistent relation to their wide range of lifestyles and hearing parameters. However, the mountain beaver, and to a lesser extent the pocket gopher, two rodents that live in tunnel systems, had relative sizes of summed granular regions and DCN molecular layer distinctly larger than those of the other mammals. Among all the mammals studied, there was a high correlation between the size per body weight of summed granular regions and that of the DCN molecular layer, consistent with other evidence for a close relationship between granule cells and superficial DCN neurons.

Sound localization in common vampire bats: acuity and use of the binaural time cue by a small mammal.

Passive sound-localization acuity and the ability to use binaural time and intensity cues were determined for the common vampire bat (Desmodus rotundus). The bats were tested using a conditioned suppression/avoidance procedure in which they drank defibrinated blood from a spout in the presence of sounds from their right, but stopped drinking (i.e., broke contact with the spout) whenever a sound came from their left, thereby avoiding a mild shock. The mean minimum audible angle for three bats for a 100-ms noise burst was 13.1°-within the range of thresholds for other bats and near the mean for mammals. Common vampire bats readily localized pure tones of 20 kHz and higher, indicating they could use interaural intensity-differences. They could also localize pure tones of 5 kHz and lower, thereby demonstrating the use of interaural time-differences, despite their very small maximum interaural distance of 60 µs. A comparison of the use of locus cues among mammals suggests several implications for the evolution of sound localization and its underlying anatomical and physiological mechanisms.

Hearing in alpacas (Vicugna pacos): audiogram, localization acuity, and use of binaural locus cues.

Behavioral audiograms and sound localization abilities were determined for three alpacas (Vicugna pacos). Their hearing at a level of 60 dB sound pressure level (SPL) (re 20 µPa) extended from 40 Hz to 32.8 kHz, a range of 9.7 octaves. They were most sensitive at 8 kHz, with an average threshold of -0.5 dB SPL. The minimum audible angle around the midline for 100-ms broadband noise was 23°, indicating relatively poor localization acuity and potentially supporting the finding that animals with broad areas of best vision have poorer sound localization acuity. The alpacas were able to localize low-frequency pure tones, indicating that they can use the binaural phase cue, but they were unable to localize pure tones above the frequency of phase ambiguity, thus indicating complete inability to use the binaural intensity-difference cue. In contrast, the alpacas relied on their high-frequency hearing for pinna cues; they could discriminate front-back sound sources using 3-kHz high-pass noise, but not 3-kHz low-pass noise. These results are compared to those of other hoofed mammals and to mammals more generally.

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/m(2)), 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.

Conditioned suppression/avoidance as a procedure for testing hearing in birds: the domestic pigeon (Columba livia).

Although the domestic pigeon is commonly used in learning experiments, it is a notoriously difficult subject in auditory psychophysical experiments, even those in which it need only respond when it detects a sound. This is because pigeons tend to respond in the absence of sound-that is, they have a high false-positive rate-which makes it difficult to determine a pigeon's audiogram. However, false positives are easily controlled in the method of conditioned suppression/avoidance, in which a pigeon is trained to peck a key to obtain food and to stop pecking whenever it detects a sound that signals impending electric shock. Here, we describe how to determine psychophysical thresholds in pigeons using a method of conditioned suppression in which avoidable shock is delivered through a bead chain wrapped around the base of a pigeon's wings. The resulting audiogram spans the range from 2 to 8000 Hz; it falls approximately in the middle of the distribution of previous pigeon audiograms and supports the finding of Kreithen and Quine (Journal of Comparative Physiology 129:1-4, 1979) that pigeons hear infrasound.

Hearing in American leaf-nosed bats. IV: the Common vampire bat, Desmodus rotundus.

We behaviorally determined the audiograms of three Common vampire bats (Phyllostomidae, Desmodus rotundus), a species specialized to exist exclusively on blood. The bats were trained to respond to pure tones in a conditioned suppression/avoidance procedure for a blood reward and a mild punisher for failures to detect the tones. Common vampire bats have a hearing range from 716 Hz to 113 kHz at a level of 60 dB. Their best hearing is at 20 kHz where they are slightly more sensitive than other bats, and they have a second peak of good sensitivity at 71 kHz. They have unusually good sensitivity to low frequencies compared to other bats, but are less sensitive to low frequencies than most mammals. Selective pressures affecting high-frequency hearing in bats and mammals in general are discussed.

Use of binaural cues for sound localization in two species of Phyllostomidae: the Greater spear-nosed bat (Phyllostomus hastatus) and the Short-tailed fruit bat (Carollia perspicillata).

Unlike humans, not all mammals use both of the binaural cues for sound localization. Whether an animal uses these cues can be determined by testing its ability to localize pure tones; specifically, low frequencies are localized using time-difference cues, and high frequencies are localized using intensity-difference cues. We determined the ability to use binaural cues in 2 New World bats, Phyllostomus hastatus, large omnivores, and Carollia perspicillata, small frugivores, by testing their tone-localization ability using a conditioned avoidance procedure. Both species easily localized high-frequency tones, indicating that they could use the interaural intensity-difference cue. However, neither species was able to use the phase-difference cue to localize either low-frequency pure tones or amplitude-modulated tones (which provided an envelope for additional time analysis). We now know of 3 bat species that cannot use binaural time cues and 2 that can. Further exploration of localization in bats may provide insight into the neural analysis of time cues in species that do not hear low frequencies.

Use of binaural cues for sound localization in large and small non-echolocating bats: Eidolon helvum and Cynopterus brachyotis.

The authors determined the ability of two old-world non-echolocating bats, Eidolon helvum and Cynopterus brachyotis, to use binaural time and intensity difference cues for localization. The bats were trained to localize pure tones throughout most of their hearing range from loudspeakers located 30 degrees to the left and right of midline. Both species easily localized high frequency tones, indicating they could use the interaural intensity difference cue. However, neither was able to localize low frequency tones even when the tones were amplitude modulated thereby indicating that they could not use ongoing phase difference cues. The authors now know of eight mammals that do not use binaural phase cues for localization, and some possible reasons for this inability are explored.

Laboratory rats (Rattus norvegicus) do not use binaural phase differences to localize sound.

The ability of Norway rats to use binaural time- and intensity-difference cues to localize sound was investigated by determining their ability to localize pure tones from 500 Hz to 32 kHz. In addition, their ability to use the binaural time cues present in the envelope of a signal was determined by presenting them with a 1-kHz tone that was amplitude modulated at either 250 or 500 Hz. Although the animals were easily able to localize tones above 2 kHz, indicating that they could use the binaural intensity-difference cue, they were virtually unable to localize the lower-frequency stimuli, indicating that they could not use the binaural phase (time) cue. Although some animals showed a residual ability to localize low-frequency tones, control tests indicated that they were using the transient interaural intensity difference in the onset of a sound that exists after it reaches the near ear but before it reaches the far ear. Thus, in contrast to earlier studies, we conclude that the Norway rat is unable to use the ongoing time cues available in low-frequency tones to localize sound, raising the possibility that the rat may not use interaural time differences to localize sound.

Comparison of behavioral and auditory brainstem response measures of threshold shift in rats exposed to loud sound.

The purpose of this study was to determine how closely the auditory brainstem response (ABR) can estimate sensorineural threshold shifts in rats exposed to loud sound. Behavioral and ABR thresholds were obtained for tones or noise before and after exposure to loud sound. The results showed that the ABR threshold shift obtained with tone pips estimated the initial pure-tone threshold shifts to within +/-5 dB 11% of the time and the permanent pure-tone threshold shifts 55% of the time, both with large errors. Determining behavioral thresholds for the same tone pips used for the ABR did not improve the agreement between the measures. In contrast, the ABR obtained with octave noise estimated the initial threshold shifts for that noise to within +/-5 dB 25% of the time and the permanent threshold shifts 89% of the time, with much smaller errors. Thus, it appears that the noise-evoked ABR is more accurate in estimating threshold shift than the tone-evoked ABR.