Gimseong Koay

Audiograms of five species of rodents: implications for the evolution of hearing and the perception of pitch

Behavioral audiograms were determined for five species of rodents: groundhog (Marmota monax), chipmunk (Tamias striatus), Darwins leaf-eared mouse (Phyllotis darwinii), golden hamster (Mesocricetus auratus), and Egyptian spiny mouse (Acomys cahirinus). The high-frequency hearing of these animals was found to vary inversely with interaural distance, a typical mammalian pattern. With regard to low-frequency hearing, the animals fell into two groups: those with extended low-frequency hearing (chipmunks, groundhogs, and hamsters hear below 100 Hz) and those with restricted low-frequency hearing (spiny and leaf-eared mice do not hear appreciably below 1 kHz). An analysis of mammalian hearing reveals that the distribution of low-frequency hearing limits is bimodal with the two distributions separated by a gap from 125 to 500 Hz. The correspondence of this dichotomy with studies of temporal coding raises the possibility that mammals that do not hear below 500 Hz do not use temporal encoding for the perception of pitch.

Cross-modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour.

Potential auditory compensation in neonatally bilaterally enucleated Syrian hamsters was explored anatomically, electrophysiologically and behaviourally. Gross morphology of the visual cortex appeared normal and no obvious cytoarchitectural malformation was discerned. However, enucleation induced a significant increase in the spontaneous firing rate of visual cortex cells. Further, auditory stimuli elicited field potentials and single unit responses in the visual cortex of enucleated, but not normal, animals. About 63% of the cells isolated in the visual cortex of 16 enucleated hamsters responded to at least one type of auditory stimulus. Most of the responses were less vigorous and less time‐locked than those of auditory cortex cells, and thresholds were typically higher. Projection tracing with WGA–HRP disclosed reciprocal connections between the visual cortex and the dorsal lateral geniculate nucleus in both intact and enucleated animals. However, in the enucleated animals retrogradely labelled cells were also found in the inferior colliculus, the major midbrain auditory nucleus. Behaviourally determined auditory sensitivity across the hearing range did not differ between enucleated and intact hamsters. Minimum audible angle, as determined by a conditioned suppression task, ranged from around 17 to 22°, with no significant difference between normal and enucleated animals. The two groups also did not differ with regard to the direction of their unconditioned head orientating response to intermittent noise. However, the enucleated animals showed a more vigorous response and were slower to habituate to the noise. These results show that bilateral enucleation of newborn hamsters results in auditory activation of visual targets, in addition to the typical activation of the intact auditory pathway. Behaviourally it appears that enucleated hamsters, compared with their normal littermates, are slower to habituate in their response to an unexpected source of sound.

Audiogram of the big brown bat (Eptesicus fuscus)

The audiograms of three big brown bats (Eptesicus fuscus) were determined using a conditioned avoidance procedure. The average audiogram ranged from 0.850 kHz at 106 dB to 120 kHz at 83 dB SPL, with a best threshold of 7 dB at 20 kHz and a distinct decrease in sensitivity at 45 kHz. The results confirm those of a previous study by Dalland (1965a) that the big brown bat has good high-frequency hearing coupled with poor low-frequency hearing. Comparative analysis suggests that the bats good high-frequency hearing initially evolved for passive sound localization and that it was later coopted for use in echolocation. In addition, the restricted low-frequency hearing of the big brown bat is typical of mammals with good high-frequency hearing.

Passive sound-localization ability of the big brown bat (Eptesicus fuscus)

The passive sound-localization ability (i.e. minimum audible angle) of the big brown bat, Eptesicus fuscus, was determined using a conditioned avoidance procedure in which the animals were trained to discriminate left sounds from right sounds. The mean threshold of three bats for a 100-ms broadband noise burst was 14 degrees, a value that is about average for mammals. A similar threshold of 15 degrees was obtained for one animal when it was retested with one of its own recorded echolocation calls as the stimulus. The two bats tested on pure-tone localization were able to localize high-frequency, but not low-frequency tones, even when a low-frequency tone was amplitude modulated, a result indicating that these bats are not able to use binaural time-difference cues for localization. Finally, given the width of the bats field of best vision, as determined by a count of its ganglion-cell density, its sound-localization acuity is consistent with the hypothesis that the role of passive sound localization is to direct the eyes to the source of a sound.

Tinnitus and hearing loss in hamsters (Mesocricetus auratus) exposed to loud sound.

Hamsters were trained to go left and right to sounds on their left and right sides, respectively. Silent trials were occasionally given in which no sound was presented. Hamsters exposed to a loud 2- or 10-kHz tone in 1 ear often shifted their responding on the silent trials to the side of the exposed ear, suggesting that they perceived a sound in that ear (i.e., tinnitus). The degree of tinnitus was related to the degree of the accompanying hearing loss (estimated by the auditory brainstem response). However, a conductive hearing loss (plugging 1 ear) did not cause a hamster to test positive for tinnitus. Tinnitus could be demonstrated within minutes following tone exposure, indicating an immediate onset, as occurs in humans.

Sound localization in a new-world frugivorous bat, Artibeus jamaicensis: Acuity, use of binaural cues, and relationship to vision

Passive sound-localization acuity and its relationship to vision were determined for the echolocating Jamaican fruit bat (Artibeus jamaicensis). A conditioned avoidance procedure was used in which the animals drank fruit juice from a spout in the presence of sounds from their right, but suppressed their behavior, breaking 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 10 degrees-marginally superior to the 11.6 degrees threshold for Egyptian fruit bats and the 14 degrees threshold for big brown bats. Jamaican fruit bats were also able to localize both low- and high-frequency pure tones, indicating that they can use both binaural phase- and intensity-difference cues to locus. Indeed, their ability to use the binaural phase cue extends up to 6.3 kHz, the highest frequency so far for a mammal. The width of their field of best vision, defined anatomically as the width of the retinal area containing ganglion-cell densities at least 75% of maximum, is 34 degrees. This value is consistent with the previously established relationship between vision and hearing indicating that, even in echolocating bats, the primary function of passive sound localization is to direct the eyes to sound sources.

Behavioral audiograms of homozygous medJ mutant mice with sodium channel deficiency and unaffected controls

Complete behavioral audiograms were determined for med(J) mice (F1 offspring of C57BL/6JxC3HeB/FeJ) and unaffected controls from the same F1 background. The med(J) mutation results in greatly reduced levels of Scn8a voltage-gated sodium channels, which causes abnormal conduction of action potentials throughout the nervous system and may account for the virtual absence of spontaneous bursting activity in the dorsal cochlear nucleus. The med(J) mice also have tremors, display dystonic postures, and drag their hind legs. The mice were tested using a conditioned suppression/avoidance procedure, with minor modifications of the apparatus made to accommodate the motor-impaired med(J) mice. Thresholds were repeatedly obtained up to the age of 50 weeks to determine if the animals developed a hearing loss with age. The results indicate that med(J) mice have normal thresholds, with the first signs of hearing loss (detectable at 80 kHz) appearing for both the med(J) and normal mice by 48 weeks. Neither the med(J) nor the normal mice could hear below 1 kHz, indicating that house mice fall into the group of mammals with poor low-frequency hearing. The results also demonstrate that the conditioned suppression/avoidance procedure is well suited for assessing hearing in severely impaired, as well as normal, mice and that it can provide for the rapid determination of thresholds necessary to follow changes in hearing that may occur as the result of age, disease, mutation, or drugs.

Sound localization in chinchillas. I: Left/right discriminations

The ability of chinchillas to localize sound was examined behaviorally using a conditioned avoidance procedure in which the animals were trained to discriminate left from right sound sources. Their minimum audible angle was 15.6 degrees for 100-ms broadband noise making them one of the more accurate rodents, although they are not as accurate as primates and carnivores. Thresholds obtained for filtered noise stimuli demonstrated that chinchillas are equally accurate in localizing either low- or high-frequency noise. Further, they are able to use both interaural phase-difference and interaural intensity-difference cues as demonstrated by their ability to localize both low- and high-frequency pure tones. Finally, analysis of the chinchilla retina supports the hypothesis that the role of auditory localization in directing the eyes to sound sources played a role in the evolution of auditory spatial perception.

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.

Hearing in American leaf-nosed bats. II: Carollia perspicillata.

We determined the audiograms of two short-tailed fruit bats (Carollia perspicillata), 18-g phyllostomids from Central and South America. For testing, we used a conditioned suppression/avoidance procedure with a fruit juice reward. At an intensity of 60 dB SPL, the hearing of C. perspicillata extends from 5.2 to 150 kHz, showing a best sensitivity of 0 dB at 25 kHz and a secondary region of sensitivity at 71 kHz. Although C. perspicillata is frugivorous and therefore does not rely on sonar for detecting and pursuing insects, its audiogram is similar to that of insectivorous bats; similarly, there is no suggestion of unusual sensitivity associated with its low-intensity echolocation calls. The behavioral audiogram is compared to previously published physiological estimates of hearing.