Mechanisms of Spectrotemporal Modulation Detection for Normal- and Hearing-Impaired Listeners

Spectrotemporal modulations (STM) are essential features of speech signals that make them intelligible. While their encoding has been widely investigated in neurophysiology, we still lack a full understanding of how STMs are processed at the behavioral level and how cochlear hearing loss impacts this processing. Here, we introduce a novel methodological framework based on psychophysical reverse correlation deployed in the modulation space to characterize the mechanisms underlying STM detection in noise. We derive perceptual filters for young normal-hearing and older hearing-impaired individuals performing a detection task of an elementary target STM (a given product of temporal and spectral modulations) embedded in other masking STMs. Analyzed with computational tools, our data show that both groups rely on a comparable linear (band-pass)–nonlinear processing cascade, which can be well accounted for by a temporal modulation filter bank model combined with cross-correlation against the target representation. Our results also suggest that the modulation mistuning observed for the hearing-impaired group results primarily from broader cochlear filters. Yet, we find idiosyncratic behaviors that cannot be captured by cochlear tuning alone, highlighting the need to consider variability originating from additional mechanisms. Overall, this integrated experimental-computational approach offers a principled way to assess suprathreshold processing distortions in each individual and could thus be used to further investigate interindividual differences in speech intelligibility.

Human Auditory-Frequency Tuning Is Sensitive to Tonal Language Experience

Purpose The aim of this study is to investigate whether human auditory frequency tuning can be influenced by tonal language experience. Method Perceptual tuning measured via psychophysical tuning curves and cochlear tuning derived via stimulus-frequency otoacoustic emission suppression tuning curves in 14 native speakers of a tonal language (Mandarin) were compared to those of 14 native speakers of a nontonal language (English) at 1 and 4 kHz. Results Group comparisons of both psychophysical tuning curves ( p = .046) and stimulus-frequency otoacoustic emission suppression tuning curves ( p = .007) in the 4-kHz region indicated sharper frequency tuning in the Mandarin-speaking group relative to the English-speaking group. The auditory tuning was better at the higher (4 kHz) than the lower (1 kHz) probe frequencies ( p < .001). Conclusions The sharper auditory tuning in the 4-kHz cochlear region is associated with long-term tonal language (i.e., Mandarin) experience. Experience-dependent plasticity of tonal language may occur before the sound signal reaches central neural stages, as peripheral as the cochlea.

Active outer hair cell motility can suppress vibrations in the organ of Corti

High sensitivity and selectivity of hearing require active cochlea. The cochlear sensory epithelium, the organ of Corti, vibrates due to external and internal excitations. The external stimulation is acoustic pressures mediated by the scala fluids, while the internal excitation is generated by a type of sensory receptor cells (the outer hair cells) in response to the acoustical vibrations. The outer hair cells are cellular actuators that are responsible for cochlear amplification. The organ of Corti is highly structured for transmitting vibrations originating from acoustic pressure and active outer hair cell force to the inner hair cells that synapse on afferent nerves. Understanding how the organ of Corti vibrates due to acoustic pressure and outer hair cell force is critical for explaining cochlear function. In this study, excised cochlear turns were freshly isolated from young gerbils. The organ of Corti in the excised cochlea was subjected to mechanical and electrical stimulation that are analogous to acoustical and cellular stimulation in the natural cochlea. Organ of Corti vibrations including those of individual outer hair cells were measured using optical coherence tomography. Respective vibration patterns due to mechanical and electrical stimulation were characterized. Interactions between the two vibration patterns were investigated by applying the two forms of stimulation simultaneously. Our results show that the interactions could be either constructive or destructive, which implies that the outer hair cells can either amplify or suppress vibrations in the organ of Corti. We discuss a potential consequence of the two interaction modes for cochlear frequency tuning.Statement of SignificanceThe function of the mammalian cochlea is characterized by sharp tuning and high-level of amplification. Both tuning and amplification are achieved mechanically through the action of cellular actuators in the sensory epithelium. According to widely accepted theory, cochlear tuning is achieved by ‘selectively amplifying’ acoustic vibrations. This study presents a set of data suggesting that the cochlear actuators can both amplify and suppress vibrations to enhance cochlear tuning. Presented results will explain why the actuator cells in the cochlea spend energy in the locations where there is no need for amplification.

Across-species differences in pitch perception are consistent with differences in cochlear filtering

Pitch perception is critical for recognizing speech, music and animal vocalizations, but its neurobiological basis remains unsettled, in part because of divergent results across species. We investigated whether species-specific differences exist in the cues used to perceive pitch and whether these can be accounted for by differences in the auditory periphery. Ferrets accurately generalized pitch discriminations to untrained stimuli whenever temporal envelope cues were robust in the probe sounds, but not when resolved harmonics were the main available cue. By contrast, human listeners exhibited the opposite pattern of results on an analogous task, consistent with previous studies. Simulated cochlear responses in the two species suggest that differences in the relative salience of the two pitch cues can be attributed to differences in cochlear filter bandwidths. The results support the view that cross-species variation in pitch perception reflects the constraints of estimating a sound’s fundamental frequency given species-specific cochlear tuning.

Swept-Tone Stimulus-Frequency Otoacoustic Emissions in Human Newborns

Several types of otoacoustic emissions have been characterized in newborns to study the maturational status of the cochlea at birth and to develop effective tests of hearing. The stimulus-frequency otoacoustic emission (SFOAE), a reflection-type emission elicited with a single low-level pure tone, is the least studied of these emissions and has not been comprehensively characterized in human newborns. The SFOAE has been linked to cochlear tuning and is sensitive to disruptions in cochlear gain (i.e., hearing loss) in adult subjects. In this study, we characterize SFOAEs evoked with rapidly sweeping tones in human neonates and consider the implications of our findings for human cochlear maturation. SFOAEs were measured in 29 term newborns within 72 hr of birth using swept tones presented at 2 oct/s across a four-octave frequency range (0.5–8 kHz); 20 normal-hearing young adults served as a control group. The prevalence of SFOAEs in newborns was as high as 90% (depending on how response “presence” was defined). Evidence of probe-tip leakage and abnormal ear-canal energy reflectance was observed in those ears with absent or unmeasurable SFOAEs. Results in the group of newborns with present stimulus-frequency emissions indicate that neonatal swept-tone SFOAEs are adult-like in morphology but have slightly higher amplitude compared with adults and longer SFOAE group delays. The origin of these nonadult-like features is probably mixed, including contributions from both conductive (ear canal and middle ear) and cochlear immaturities.

Mammalian behavior and physiology converge to confirm sharper cochlear tuning in humans

Frequency analysis of sound by the cochlea is the most fundamental property of the auditory system. Despite its importance, the resolution of this frequency analysis in humans remains controversial. The controversy persists because the methods used to estimate tuning in humans are indirect and have not all been independently validated in other species. Some data suggest that human cochlear tuning is considerably sharper than that of laboratory animals, while others suggest little or no difference between species. We show here in a single species (ferret) that behavioral estimates of tuning bandwidths obtained using perceptual masking methods, and objective estimates obtained using otoacoustic emissions, both also employed in humans, agree closely with direct physiological measurements from single auditory-nerve fibers. Combined with human behavioral data, this outcome indicates that the frequency analysis performed by the human cochlea is of significantly higher resolution than found in common laboratory animals. This finding raises important questions about the evolutionary origins of human cochlear tuning, its role in the emergence of speech communication, and the mechanisms underlying our ability to separate and process natural sounds in complex acoustic environments.

Pitch perception is adapted to species-specific cochlear filtering

Pitch perception is critical for recognizing speech, music and animal vocalizations, but its neurobiological basis remains unsettled, in part because of divergent results from different species. We used a combination of behavioural measurements and cochlear modelling to investigate whether species-specific differences exist in the cues used to perceive pitch and whether these can be accounted for by differences in the auditory periphery. Ferrets performed a pitch discrimination task well whenever temporal envelope cues were robust, but not when resolved harmonics only were available. By contrast, human listeners exhibited the opposite pattern of results on an analogous task, consistent with previous studies. Simulated cochlear responses in the two species suggest that the relative salience of the two types of pitch cues can be attributed to differences in cochlear filter bandwidths. Cross-species variation in pitch perception may therefore reflect the constraints of estimating a sound’s fundamental frequency given species-specific cochlear tuning.

LMO7 deficiency reveals the significance of the cuticular plate for hearing function

Sensory hair cells, the mechanoreceptors of the auditory and vestibular system, harbor two specialized organelles, the hair bundle and the cuticular plate. Both subcellular structures have adapted to facilitate the remarkable sensitivity and speed of hair cell mechanotransduction. While the mechanosensory hair bundle is extensively studied, the molecules and mechanisms mediating the development and function of the cuticular plate are poorly understood. The cuticular plate is believed to provide a rigid foundation for stereociliar pivot movements, but specifics about its function, especially the significance of its integrity for long-term maintenance of hair cell mechanotransduction, are not known. In this study, we describe the discovery of a hair cell protein called LIM only protein 7 (LMO7). In the hair cell, LMO7 is specifically localized in the cuticular plate. Lmo7 KO mice suffer multiple deficiencies in the cuticular plate, including reduced filamentous actin density and abnormal length and distribution of stereociliar rootlets. In addition to the cuticular plate defects, older Lmo7 KO mice develop abnormalities in inner hair cell stereocilia. Together, these defects affect cochlear tuning and sensitivity and give rise to late-onset progressive hearing loss.