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Sugai, J. A.

Publications and source records attributed to Sugai, J. A..

5 recordsLinked to original sources

Neural and autonomic predictors of future listening errors

Some of the most demanding perceptual tasks require sustained vigilance to detect and classify infrequent, unpredictable targets within continuous sensory streams. Here, we designed a sustained listening task to ask whether cardinal classes of perceptual errors (misclassifications, miss, and false alarms) were associated with variability in event-related processing, ongoing cortical state, and autonomic arousal. We recorded 64-channel scalp EEG and pupil diameter in 39 adults while they monitored streams of random tone pips for occasional target sequences of repeating tones. A target-evoked negativity varied systematically with listening outcome: it was largest for correct reports, reduced for misclassifications, and nearly absent for misses. Notably, these differences emerged within the first 500 ms of the target sequence, before the information needed to classify its length was available. Related negativities also accompanied false alarms despite the absence of a target. By contrast, neural synchronization to acoustic cues in individual tone pips did not differ across perceptual outcomes. We then looked further back in time, to the 1 s period preceding target onset, and identified additional signatures of forthcoming misclassifications and false alarms in pupil diameter and EEG aperiodic slopes. Models evaluated with leave-one-subject-out cross-validation showed that baseline state measures and event-related negativity amplitude provided complementary information about the probability and type of forthcoming errors. These findings link perceptual errors during sustained listening to higher-order cortical and arousal-state dynamics rather than fluctuant encoding of bottom-up acoustic cues.

neuroscience↗

Perceptual and neural biomarkers of distraction from an external sound source are not associated with tinnitus severity

Individuals with chronic tinnitus perceive a phantom sound that imposes either a bothersome and irrepressible distraction throughout waking hours or a relatively mild nuisance that often fades into subliminal awareness. The difference in tinnitus salience may reflect a general difference in inhibitory control over any distracting sound, whether externally or internally generated. To test this hypothesis, we investigated neural and behavioral signatures of external auditory distraction suppression in participants with chronic tinnitus that had mild or bothersome tinnitus but were otherwise matched for age and hearing loss. Participants in both groups underwent behavioral and EEG testing that asked them to report on a target stream of amplitude modulated tones that switched from a random arrangement to a repeating sequence. Using additional sounds that imposed varying levels of distraction, we documented neural and perceptual suppression of auditory distractors. Behaviorally, participants with mild versus bothersome tinnitus showed comparable reductions in accuracy in the presence of varying distractor loads. Neural synchronization to the target stimulus change rate provided a useful proxy for distraction effects but did not differ between tinnitus groups. Likewise, no group differences were observed in the neural synchronization to modulation rates of the target or distractor stimuli. Our results build on work showing that individuals with tinnitus perform as well as individuals with normal hearing on listening tasks in noisy environments and expand this observation into the neural representation of sounds. Suppression of the internally generated phantom percept does not appear to be linked to general deficits in suppressing distractors.

neuroscience↗

Arousal state fluctuations are a source of internal noise underlying age-related declines in speech intelligibility

Understanding speech in noisy, multi-talker environments is crucial for social communication but becomes increasingly challenging and frustrating as we age. Here, we simulated the acoustic challenges of multi-talker listening and found that adults over 50 years old (N = 76) recognized speech more slowly, less accurately, and less consistently than younger adults (N = 107). While peripheral hearing status accounted for average differences in speech intelligibility by age, it did not account for moment-to-moment variability in speed and accuracy - fluctuations central to the frustration experienced by older listeners in challenging environments. We hypothesized that age-related changes in brain arousal systems might account for the fluctuant "noise" in speech processing observed in older listeners. To isolate the contribution of arousal state independent of hearing status and cognitive load, we measured the pre-stimulus pupil-indexed arousal state (PPAS) immediately prior to speech onset. Older - but not younger - adults exhibited a striking inverted-U relationship between PPAS and speech recognition accuracy. Notably, pupil-indexed listening effort measured seconds later during speech encoding was not associated with trial-to-trial performance. Moreover, older adults exhibited altered arousal regulation, occupying a lower PPAS extremum not observed in younger listeners that was specifically associated with performance deficits and subjective listening difficulties reported in hearing health questionnaires. These findings show that age-related changes in central arousal states interact with peripheral hearing status to offer a more complete explanation for why older adults find speech processing in social setting so challenging. Significance StatementAs we age, following a conversation in crowded environments becomes more difficult and frustrating, even when hearing tests appear normal. This study shows that variations in arousal level (measured through pre-stimulus pupil size) are tightly linked to fluctuations in the speed and accuracy of speech processing in adults over 50 years of age. Changes in arousal state regulation uniquely accounted for the moment-to-moment variations in speech intelligibility and were more closely associated with self-reported listening challenges than other conventional measures. These findings highlight the contribution of brain-wide arousal systems to real-world listening challenges and identify a straightforward measure that could be used to more comprehensively assess and potentially improve speech understanding in social settings.

neuroscience↗

The Slowest Timescales of Neural Synchronization Reveal the Strongest Influence of Auditory Distraction

Among all the sounds occurring at any given time, people are often interested in listening to just one. Some competing sounds are merely background noise, whereas others distract attention from target sounds and are less easily suppressed. During active listening, the central auditory pathway unmixes target and distractor sounds based on temporal differences that vary across three orders of magnitude - from millisecond differences in acoustic temporal fine structure to slower perceptual grouping factors that stretch out to multiple seconds. Here, we developed an approach to directly measure central auditory encoding of multiplexed target and distractor sound features in human listeners to determine which timescales are most impacted by the presence of distracting sounds. Target sounds contained nested features along four timescales, including temporal fine structure ([~]500 Hz), temporal envelope ([~]25-80 Hz), envelope changes ([~]5 Hz), and slower changes in embedded context reflecting whether target stimuli were randomly arranged or formed a repeating pattern ([~]0.5 Hz). Targets were presented with competing sounds that provided variable levels of distraction: either a highly distracting melody or a less distracting noise. Neural synchronization to each timescale was simultaneously and independently measured for target and distractor sounds from electroencephalogram (EEG) recordings during a listening task. Sustained shifts from random to regular arrangements of temporal sequences were reliably perceived, yet did not evoke a pattern recognition potential, nor neural synchronization changes at any timescale. Synchronization to relatively slow changes in envelope transitions (<10Hz) of the target sound deteriorated with the addition of a more distracting sound while synchronization to more rapid fluctuations in the fine structure or envelope modulation rate were unaffected by varying levels of distraction. Categorizing trials according to task performance revealed a conjunction of enhanced entrainment to slower temporal features in the distractor sound and reduced synchronization to the target sound on error trials. By designing a stimulus paradigm that leveraged the remarkable temporal processing capabilities of the auditory nervous system, we were able to simultaneously quantify multiple target and distractor sound features reproduced in the EEG. This paradigm identified synchronization processes in the 7-10 Hz alpha range that has been linked to distractor suppression, which may prove valuable for research on clinical populations who report difficulty suppressing awareness of distracting sounds.

neuroscience↗

The human pupil and face encode sound affect and provide objective signatures of tinnitus and auditory hypersensitivity disorders

Sound is jointly processed along acoustic and emotional dimensions. These dimensions can become distorted and entangled in persons with sensory disorders, producing a spectrum of loudness hypersensitivity, phantom percepts, and - in some cases - debilitating sound aversion. Here, we looked for objective signatures of disordered hearing (DH) in the human face. Pupil dilations and micro facial movement amplitudes scaled with sound valence in neurotypical listeners but not DH participants with chronic tinnitus (phantom ringing) and sound sensitivity. In DH participants, emotionally evocative sounds elicited abnormally large pupil dilations but blunted and invariant facial reactions that jointly provided an accurate prediction of individual tinnitus and hyperacusis questionnaire handicap scores. By contrast, EEG measures of central auditory gain identified steeper neural response growth functions but no association with symptom severity. These findings highlight dysregulated affective sound processing in persons with bothersome tinnitus and sound sensitivity disorders and introduce approaches for their objective measurement.

neuroscience↗