Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

Henry, Kenneth S.; Abrams, Kristina S.; Forst, Johanna; Mender, Matthew J; Neilans, Erikson G.; Idrobo, Fabio; Carney, Laurel H.

doi:10.1007/s10162-016-0594-4

Cited by 30 publications

(30 citation statements)

References 66 publications

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“…These results suggest that both rate and synchronization representation of periodicity might exist at the level of the IC. Henry et al (2017) also showed that IC neurons in awake budgerigar encoded the vowel-like sounds by the neural synchrony and variations in average discharge rate related the envelope structure. Studies of the correlation between the behaviourally measured sensitivity to amplitude-modulated signals and neural responses in the IC showed that the synchronized temporal representation was more correlated with behavioral performance than rate representation for envelope detection in awake budgerigar ( Henry et al, 2016 ).…”

Section: Discussionmentioning

confidence: 92%

Temporal Coding of Voice Pitch Contours in Mandarin Tones

Peng

Innes‐Brown

McKay

et al. 2018

Front. Neural Circuits

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Accurate perception of time-variant pitch is important for speech recognition, particularly for tonal languages with different lexical tones such as Mandarin, in which different tones convey different semantic information. Previous studies reported that the auditory nerve and cochlear nucleus can encode different pitches through phase-locked neural activities. However, little is known about how the inferior colliculus (IC) encodes the time-variant periodicity pitch of natural speech. In this study, the Mandarin syllable /ba/ pronounced with four lexical tones (flat, rising, falling then rising and falling) were used as stimuli. Local field potentials (LFPs) and single neuron activity were simultaneously recorded from 90 sites within contralateral IC of six urethane-anesthetized and decerebrate guinea pigs in response to the four stimuli. Analysis of the temporal information of LFPs showed that 93% of the LFPs exhibited robust encoding of periodicity pitch. Pitch strength of LFPs derived from the autocorrelogram was significantly (p < 0.001) stronger for rising tones than flat and falling tones. Pitch strength are also significantly increased (p < 0.05) with the characteristic frequency (CF). On the other hand, only 47% (42 or 90) of single neuron activities were significantly synchronized to the fundamental frequency of the stimulus suggesting that the temporal spiking pattern of single IC neuron could encode the time variant periodicity pitch of speech robustly. The difference between the number of LFPs and single neurons that encode the time-variant F0 voice pitch supports the notion of a transition at the level of IC from direct temporal coding in the spike trains of individual neurons to other form of neural representation.

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Section: Discussionmentioning

confidence: 92%

Temporal Coding of Voice Pitch Contours in Mandarin Tones

Peng

Innes‐Brown

McKay

et al. 2018

Front. Neural Circuits

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“…Degraded midbrain response synchrony in mice with profound AN loss also suggest the possibility of impaired envelope sensitivity (Chambers et al, 2016). Future behavioral experiments in the budgerigar may provide special insight into these open questions, considering previous work on complexsound perception in this species (Carney et al, 2013;Dent et al, 2000;Dooling et al, 2000;Dooling and Searcy, 1981;Henry et al, 2017bHenry et al, , 2017aHenry et al, , 2016Okanoya and Dooling, 1987) and evidence of increased central gain after KA exposure (Henry and Abrams, 2018).…”

Section: Discussionmentioning

confidence: 97%

“…Experiments were performed in four matching acoustic test chambers (Industrial Acoustics; 0.30 m 3 ) lined with sound-absorbing foam (see Henry et al, 2017bHenry et al, , 2017aHenry et al, , 2016 detailed behavioral methods). Each chamber contained an overhead loudspeaker (Polk Audio MC60), house light, and a video camera for monitoring the animal's behavior.…”

Section: Behavioral Experimentsmentioning

confidence: 99%

“…The budgerigar (Melopsittacus undulatus) is a highly vocal avian species with human-like behavioral sensitivity to many simple and complex sounds and the capacity to mimic speech. Budgerigars have sensitive hearing from 0.25-6 kHz (Dooling and Saunders, 1975) and behavioral thresholds similar to humans on numerous psychoacoustic tasks including tonein-noise detection (Okanoya and Dooling, 1987), frequency discrimination of tones and vowel formants (Dent et al, 2000;Henry et al, 2017bHenry et al, , 2017a, amplitude modulation detection (Carney et al, 2013;Dooling and Searcy, 1981;Henry et al, 2016), and gap detection (Dooling et al, 2000). We recently developed new methods in the budgerigar to induce permanent AN damage with kainic acid (KA) (Henry and Abrams, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar

et al. 2019

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Auditory-nerve fibers are lost steadily with age and as a possible consequence of noise-induced glutamate excitotoxicity. Auditory-nerve loss in the absence of other cochlear pathologies is thought to be undetectable with a pure-tone audiogram while degrading real-world speech perception (hidden hearing loss). Perceptual deficits remain unclear, however, due in part to the limited behavioral capacity of existing rodent models to discriminate complex sounds. The budgerigar is an avian vocal learner with human-like behavioral sensitivity to many simple and complex sounds and the capacity to mimic speech. Previous studies in this species show that intracochlear kainic-acid infusion reduces wave 1 of the auditory brainstem response by 40-70%, consistent with substantial excitotoxic auditory-nerve damage. The present study used operantconditioning procedures in trained budgerigars to quantify kainic-acid effects on tone detection across frequency (0.25-8 kHz; the audiogram) and as a function of duration (20-160 ms; temporal integration). Tone thresholds in control animals were lowest from 1-4 kHz and decreased with increasing duration as in previous studies of the budgerigar. Behavioral results in kainic-acidexposed animals were as sensitive as in controls, suggesting preservation of the audiogram and temporal integration despite auditory-nerve loss associated with up to 70% wave 1 reduction. Distortion-product otoacoustic emissions were also preserved in kainic-acid exposed animals, consistent with normal hair-cell function. These results highlight considerable perceptual resistance of tone-detection performance with selective auditory-nerve loss. Future behavioral studies in budgerigars with auditory-nerve damage can use complex speech-like stimuli to help clarify aspects of auditory perception impacted by this common cochlear pathology.

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“…The temporal response properties of the midbrain neurons convey additional information related to both the formant locations and f0. This temporal information in midbrain responses is important in explaining formant discrimination thresholds in a noise background in the parakeet, an animal model that has discrimination thresholds comparable to human listeners (Henry et al, 2017). Future studies of the representations of vowels using these computational models should include both average rate and temporal response metrics.…”

Section: Resultsmentioning

confidence: 99%

Nonlinear auditory models yield new insights into representations of vowels

Carney

McDonough

2018

Atten Percept Psychophys

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Studies of vowel systems regularly appeal to the need to understand how the auditory system encodes and processes the information in the acoustic signal. The goal of this study is to present computational models to address this need, and to use the models to illustrate responses to vowels at two levels of the auditory pathway. Many of the models previously used to study auditory representations of speech are based on linear filter banks simulating the tuning of the inner ear. These models do not incorporate key nonlinear response properties of the inner ear that influence responses at conversational-speech sound levels. These nonlinear properties shape neural representations in ways that are important for understanding responses in the central nervous system. The model for auditory-nerve (AN) fibers used here incorporates realistic nonlinear properties associated with the basilar membrane, inner hair cells (IHCs), and the IHC-AN synapse. These nonlinearities set up profiles of f0-related fluctuations that vary in amplitude across the population of frequency-tuned AN fibers. Amplitude fluctuations in AN responses are smallest near formant peaks and largest at frequencies between formants. These f0-related fluctuations strongly excite or suppress neurons in the auditory midbrain, the first level of the auditory pathway where tuning for low-frequency fluctuations in sounds occurs. Formant-related amplitude fluctuations provide representations of the vowel spectrum in discharge rates of midbrain neurons. These representations in the midbrain are robust across a wide range of sound levels, including the entire range of conversational-speech levels, and in the presence of realistic background noise levels.

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Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

Cited by 30 publications

References 66 publications

Temporal Coding of Voice Pitch Contours in Mandarin Tones

Temporal Coding of Voice Pitch Contours in Mandarin Tones

Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar

Nonlinear auditory models yield new insights into representations of vowels

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