Frequency selectivity in the inner ear is fundamental to hearing and is traditionally thought to be similar across mammals. Although direct measurements are not possible in humans, estimates of frequency tuning based on noninvasive recordings of sound evoked from the cochlea (otoacoustic emissions) have suggested substantially sharper tuning in humans but remain controversial. We report measurements of frequency tuning in macaque monkeys, OldWorld primates phylogenetically closer to humans than the laboratory animals often taken as models of human hearing (e.g., cats, guinea pigs, chinchillas). We find that measurements of tuning obtained directly from individual auditory-nerve fibers and indirectly using otoacoustic emissions both indicate that at characteristic frequencies above about 500 Hz, peripheral frequency selectivity in macaques is significantly sharper than in these common laboratory animals, matching that inferred for humans above 4-5 kHz. Compared with the macaque, the human otoacoustic estimates thus appear neither prohibitively sharp nor exceptional. Our results validate the use of otoacoustic emissions for noninvasive measurement of cochlear tuning and corroborate the finding of sharp tuning in humans. The results have important implications for understanding the mechanical and neural coding of sound in the human cochlea, and thus for developing strategies to compensate for the degradation of tuning in the hearing-impaired.auditory filters | comparative hearing S ound waveforms consist of pressure fluctuations in time and space. In the process of transducing mechanical vibrations into neural signals, the cochlea performs a mechanical frequency analysis that decomposes sounds into constituent frequencies (1, 2). The frequency tuning of the cochlear filters plays a critical role in the ability to distinguish and segregate different sounds perceptually. For example, sounds that radiate from different sources superpose in the air, and are thus "mixed up" before striking the eardrums. Based on the output of the cochlear filters, and by comparing responses from the two ears, the nervous system is capable of disentangling the various sounds, grouping related frequency components to identify auditory objects and localize their sources in space (3). The critical role of peripheral frequency selectivity is perhaps best illustrated by the consequences of damage to the inner ear, which typically leads to a degradation of the cochlear filters. The loss of sharp filtering results in an impaired ability to detect signals in noise and to separate different sounds (4). Frequency selectivity is therefore crucial to everyday human communication.The study of the cochlea is hampered by its fragility and inaccessibility. Direct measurements of mechanical or neural frequency tuning in healthy cochleae are only possible in laboratory animals. To date, measurements of the mechanical vibration of the cochlea's basilar membrane have been largely restricted to the basal high-frequency end of the cochlea, where surgical acce...
The anterior intraparietal area (AIP) of macaques contains neurons that signal the depth structure of disparity-defined 3-D shapes. Previous studies have suggested that AIP's depth information is used for sensorimotor transformations related to the efficient grasping of 3-D objects. We trained monkeys to categorize disparity-defined 3-D shapes and examined whether neuronal activity in AIP may also underlie pure perceptual categorization behavior. We first show that neurons with a similar 3-D shape preference cluster in AIP. We then demonstrate that the monkeys' 3-D shape discrimination performance depends on the position in depth of the stimulus and that this performance difference is reflected in the activity of AIP neurons. We further reveal correlations between the neuronal activity in AIP and the subject's subsequent choices and RTs during 3-D shape categorization. Our findings propose AIP as an important processing stage for 3-D shape perception.
Stimulus-locked temporal codes are increasingly seen as relevant to perception. The timing of action potentials typically varies with stimulus intensity, and the invariance of temporal representations with intensity is therefore an issue. We examine the timing of action potentials in cat auditory nerve to broadband noise presented at different intensities, using an analysis inspired by coincidence detection and by the binaural "latency hypothesis." It is known that the two cues for azimuthal sound localization, interaural intensity or level differences and interaural time differences (ITDs), interact perceptually. According to the latency hypothesis, the increase in intensity for the ear nearest to a sound source off the midline causes a decrease in response latency in that ear relative to the other ear. We found that changes in intensity cause small but systematic shifts in the ongoing timing of responses in the auditory nerve, generally but not always resulting in shorter delays between stimulus onset and neural response for increasing intensity. The size of the temporal shifts depends on characteristic frequency with a pattern indicating a fine-structure and an envelope response regime. Overall, the results show that ongoing timing is remarkably stable with intensity at the most peripheral neural level. The results are not consistent in a simple way with the latency hypothesis, but because of the acute sensitivity to ITDs, the subtle effects of intensity on timing may nevertheless have perceptual consequences.
Otoacoustic estimates of cochlear frequency selectivity suggest substantially sharper tuning in humans. However, the logic and methodology underlying these estimates remain untested by direct measurements in primates. We report measurements of frequency tuning in macaque monkeys, Old-World primates phylogenetically closer to humans than the small laboratory animals often taken as models of human hearing (e.g., cats, guinea pigs, and chinchillas). We find that measurements of tuning obtained directly from individual nerve fibers and indirectly using otoacoustic emissions both indicate that peripheral frequency selectivity in macaques is significantly sharper than in small laboratory animals, matching that inferred for humans at high frequencies. Our results validate the use of otoacoustic emissions for noninvasive measurement of cochlear tuning and corroborate the finding of sharper tuning in humans.
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