Micheal L. Dent

Hearing in Birds and Reptiles

The comparative hearing of birds and reptiles should always be considered together. It is clear from the vertebrate fossil record that birds and reptiles split over 200 million years ago from the diapsid reptiles of the early Triassic period (Fedducia 1980; Carroll 1987). Because of this common ancestry, there is considerable similarity between the hearing organs of modern day birds and reptiles, especially the Crocodilia (Manley and Gleich 1991; Manley, Chapter 4). However, comparisons between reptiles and birds are difficult for a number of reasons. In reptiles, the auditory anatomy is extraordinarily diverse. While this presents investigators with excellent opportunities to understand the relation between form and function, direct data on the behavior of hearing in reptiles are almost nonexistent. This leaves our understanding of hearing in this group of vertebrates entirely based on indirect measures from anatomy and physiology. Thus, any comparison of hearing between reptiles and birds is somewhat unbalanced because it also involves a comparison across methodologies: hearing estimates from anatomical and physiological data in the case of reptiles along with behavioral estimates of hearing capabilities in birds.

Auditory temporal resolution in birds: Discrimination of harmonic complexes

The ability of three species of birds to discriminate among selected harmonic complexes with fundamental frequencies varying from 50 to 1000 Hz was examined in behavioral experiments. The stimuli were synthetic harmonic complexes with waveform shapes altered by component phase selection, holding spectral and intensive information constant. Birds were able to discriminate between waveforms with randomly selected component phases and those with all components in cosine phase, as well as between positive and negative Schroeder-phase waveforms with harmonic periods as short as 1-2 ms. By contrast, human listeners are unable to make these discriminations at periods less than about 3-4 ms. Electrophysiological measures, including cochlear microphonic and compound action potential measurements to the same stimuli used in behavioral tests, showed differences between birds and gerbils paralleling, but not completely accounting for, the psychophysical differences observed between birds and humans. It appears from these data that birds can hear the fine temporal structure in complex waveforms over very short periods. These data show birds are capable of more precise temporal resolution for complex sounds than is observed in humans and perhaps other mammals. Physiological data further show that at least part of the mechanisms underlying this high temporal resolving power resides at the peripheral level of the avian auditory system.

Avian species differences in susceptibility to noise exposure.

Previous studies of hair cell regeneration and hearing recovery in birds after acoustic overstimulation have involved relatively few species. Studies of the effects of acoustic overexposure typically report high variability. Though it is impossible to tell, the data so far also suggest there may be considerable species differences in the degree of damage and the time course and extent of recovery. To examine this issue, we exposed four species of birds (quail, budgerigars, canaries, and zebra finches) to identical conditions of acoustic overstimulation and systematically analyzed changes in hearing sensitivity, basilar papilla morphology, and hair cell number. Quail and budgerigars showed the greatest susceptibility to threshold shift and hair cell loss after overstimulation with either pure tone or bandpass noise, while identical types of overstimulation in canaries and zebra finches resulted in much less of a threshold shift and a smaller, more diffuse hair cell loss. All four species showed some recovery of threshold sensitivity and hair cell number over time. Canary and zebra finch hearing and hair cell number recovered to within normal limits while quail and budgerigars continued to have an approximately 20 dB threshold shift and incomplete recovery of hair cell number. In a final experiment, birds were exposed to identical wide-band noise overstimulation under conditions of artificial middle ear ventilation. Hair cell loss was substantially increased in both budgerigars and canaries suggesting that middle ear air pressure regulation and correlated changes in middle ear transfer function are one factor influencing susceptibility to acoustic overstimulation in small birds.

Cortical interference effects in the cocktail party problem

Humans and animals must often discriminate between complex natural sounds in the presence of competing sounds (maskers). Although the auditory cortex is thought to be important in this task, the impact of maskers on cortical discrimination remains poorly understood. We examined neural responses in zebra finch (Taeniopygia guttata) field L (homologous to primary auditory cortex) to target birdsongs that were embedded in three different maskers (broadband noise, modulated noise and birdsong chorus). We found two distinct forms of interference in the neural responses: the addition of spurious spikes occurring primarily during the silent gaps between song syllables and the suppression of informative spikes occurring primarily during the syllables. Both effects systematically degraded neural discrimination as the target intensity decreased relative to that of the masker. The behavioral performance of songbirds degraded in a parallel manner. Our results identify neural interference that could explain the perceptual interference at the heart of the cocktail party problem.

Perception of synthetic /ba/–/wa/ speech continuum by budgerigars (Melopsittacus undulatus)

Other than humans, extensive vocal learning has only been widely demonstrated in birds. Moreover, there are only a handful of avian species that are known to be good mimics of human speech. One such species is the budgerigar (Melopsittacus undulatus), which is a popular mimic of human speech and learns new vocalizations throughout adult life. Using operant conditioning procedures with a repeating background task, we tested budgerigars on the discrimination of tokens from two synthetic /ba/-/wa/ speech continua that differed in syllable, but not transition, duration. Budgerigars showed a significant improvement in discrimination performance on both continua near the phonetic boundary for humans. Budgerigars also showed a shift in the location of the phonetic boundary with a change in syllable length, similar to what has been described for humans and other primates. These results on a nonmammalian species provide support for the operation of a general, nonphonetic, auditory process as one mechanism which can lead to the well-known stimulus-length effect in humans.

The precedence effect in three species of birds (Melopsittacus undulatus, Serinus canaria, and Taeniopygia guttata).

The perceived locations of paired auditory images, simulating direct sounds and their echoes, have been recently studied in budgerigars (Melopsittacus undulatus; M. L. Dent & R. J. Dooling, 2003a, 2003b). In this article, the authors extend those experiments to include measurements of the precedence effect using a discrimination paradigm in two additional bird species: canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). Although time courses of summing localization, localization dominance, and echo thresholds were similar across all species, budgerigars had slightly higher overall levels of discrimination. The results from these experiments add further support that the precedence effect in birds is similar to that found in other animals and that the ability to suppress echoes that might degrade localization and auditory object perception may be a general property of the vertebrate auditory system.

Discrimination of ultrasonic vocalizations by CBA/CaJ mice (Mus musculus) is related to spectrotemporal dissimilarity of vocalizations.

The function of ultrasonic vocalizations (USVs) produced by mice (Mus musculus) is a topic of broad interest to many researchers. These USVs differ widely in spectrotemporal characteristics, suggesting different categories of vocalizations, although this has never been behaviorally demonstrated. Although electrophysiological studies indicate that neurons can discriminate among vocalizations at the level of the auditory midbrain, perceptual acuity for vocalizations has yet to be determined. Here, we trained CBA/CaJ mice using operant conditioning to discriminate between different vocalizations and between a spectrotemporally modified vocalization and its original version. Mice were able to discriminate between vocalization types and between manipulated vocalizations, with performance negatively correlating with spectrotemporal similarity. That is, discrimination performance was higher for dissimilar vocalizations and much lower for similar vocalizations. The behavioral data match previous neurophysiological results in the inferior colliculus (IC), using the same stimuli. These findings suggest that the different vocalizations could carry different meanings for the mice. Furthermore, the finding that behavioral discrimination matched neural discrimination in the IC suggests that the IC plays an important role in the perceptual discrimination of vocalizations.

Spatial Unmasking of Birdsong in Zebra Finches (Taeniopygia guttata) and Budgerigars (Melopsittacus undulatus)

Budgerigars and zebra finches were tested, using operant conditioning techniques, on their ability to identify a zebra finch song in the presence of a background masker emitted from either the same or a different location as the signal. Identification thresholds were obtained for three masker types differing in their spectrotemporal characteristics (noise, modulated noise, and a song chorus). Both bird species exhibited similar amounts of spatial unmasking across the three masker types. The amount of unmasking was greater when the masker was played continuously compared to when the target and masker were presented simultaneously. These results suggest that spatial factors are important for birds in the identification of natural signals in noisy environments.

Investigations of the precedence effect in budgerigars: Effects of stimulus type, intensity, duration, and location

Auditory experiments on the localization of sounds in the presence of reflections, or echoes, that arrive later and from different directions are important to understanding hearing in natural environments. The perceived location of the auditory image can change with the time delay between the presentations of a leading and lagging sound. These changes in perceived location, encompassing the precedence effect, have been examined behaviorally or physiologically in humans and a number of animals. Here, these results are extended to include budgerigars. Behavioral methods were used to measure the discrimination performance between a stimulus presented at + and - 90 degrees azimuth with a delay (left-right), from the same two stimuli presented with the opposite delay (right-left). At short delays, where humans experience summing localization, budgerigars have difficulty discriminating between the two presentation types. With increasing delays, where humans experience localization dominance, budgerigars show improved discrimination performance. At even longer delays, where echo thresholds are found in humans, discrimination performance worsens again. The shapes of the discrimination functions are affected by the intensity, locations, and durations of the stimuli, and are subject to a buildup effect. These results show that budgerigars exhibit the phases of the precedence effect similar to humans and other animals.

HEARING AND VOCALIZATIONS OF WILD-CAUGHT AUSTRALIAN BUDGERIGARS (MELOPSITTACUS UNDULATUS)

This study examined the hearing and contact calls of wild-caught Australian budgerigars (Melopsittacus undulatus) and compared these data to hearing and vocalizations in the much more extensively studied domesticated budgerigar. The spectral energy in the contact calls of both wild-caught and domesticated budgerigars falls almost exclusively in the frequency of 2-4 kHz. Absolute and masked thresholds were similar in both groups of birds. Similar to the results found in domesticated birds, critical ratio functions for the wild-caught budgerigars decreased at frequencies of 1.0 kHz-2.86 kHz and then increased again dramatically at frequencies above 2.86 kHz.