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Presacco, A.

Publications and source records attributed to Presacco, A..

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Effects of Aging on Cortical Representations of Continuous Speech

Understanding speech in a noisy environment is crucial in day-to-day interactions, and yet becomes more challenging with age, even for healthy aging. Age-related changes in the neural mechanisms that enable speech-in-noise listening have been investigated previously; however, the extent to which age affects the timing and fidelity of encoding of target and interfering speech streams are not well understood. Using magnetoencephalography (MEG), we investigated how continuous speech is represented in auditory cortex in the presence of interfering speech, in younger and older adults. Cortical representations were obtained from neural responses that time-locked to the speech envelopes using speech envelope reconstruction and temporal response functions (TRFs). TRFs showed three prominent peaks corresponding to auditory cortical processing stages: early ([~]50 ms), middle ([~]100 ms) and late ([~]200 ms). Older adults showed exaggerated speech envelope representations compared to younger adults. Temporal analysis revealed both that the age-related exaggeration starts as early as [~]50 ms, and that older adults needed a substantially longer integration time window to achieve their better reconstruction of the speech envelope. As expected, with increased speech masking, envelope reconstruction for the attended talker decreased and all three TRF peaks were delayed, with aging contributing additionally to the reduction. Interestingly, for older adults the late peak was delayed, suggesting that this late peak may receive contributions from multiple sources. Together these results suggest that there are several mechanisms at play compensating for age-related temporal processing deficits at several stages, but which are not able to fully reestablish unimpaired speech perception. NEW & NOTEWORTHYWe observed age-related changes in cortical temporal processing of continuous speech that may be related to older adults difficulty understanding speech in noise. These changes occur in both timing and strength of the speech representations at different cortical processing stages, and depend on both noise condition and selective attention. Critically, their dependency on noise condition changes dramatically among the early, middle, and late cortical processing stages, underscoring how aging differentially affects these stages.

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High Frequency Cortical Processing of Continuous Speech in Younger and Older Listeners

Neural processing along the ascending auditory pathway is often associated with a progressive reduction in characteristic processing rates. For instance, the well-known frequency-following response (FFR) of the auditory midbrain, as measured with electroencephalography (EEG), is dominated by frequencies from [~]100 Hz to several hundred Hz, phase-locking to the acoustic stimulus at those frequencies. In contrast, cortical responses, whether measured by EEG or magnetoencephalography (MEG), are typically characterized by frequencies of a few Hz to a few tens of Hz, time-locking to acoustic envelope features. In this study we investigated a crossover case, cortically generated responses time-locked to continuous speech features at FFR-like rates. Using MEG, we analyzed responses in the high gamma range of 70-200 Hz to continuous speech using neural source-localized reverse correlation and the corresponding temporal response functions (TRFs). Continuous speech stimuli were presented to 40 subjects (17 younger, 23 older adults) with clinically normal hearing and their MEG responses were analyzed in the 70-200 Hz band. Consistent with the relative insensitivity of MEG to many subcortical structures, the spatiotemporal profile of these response components indicated a cortical origin with [~]40 ms peak latency and a right hemisphere bias. TRF analysis was performed using two separate aspects of the speech stimuli: a) the 70-200 Hz carrier of the speech, and b) the 70-200 Hz temporal modulations in the spectral envelope of the speech stimulus. The response was dominantly driven by the envelope modulation, with a much weaker contribution from the carrier. Age-related differences were also analyzed to investigate a reversal previously seen along the ascending auditory pathway, whereby older listeners show weaker midbrain FFR responses than younger listeners, but, paradoxically, have stronger cortical low frequency responses. In contrast to both these earlier results, this study did not find clear age-related differences in high gamma cortical responses to continuous speech. Cortical responses at FFR-like frequencies shared some properties with midbrain responses at the same frequencies and with cortical responses at much lower frequencies. HighlightsO_LICortical MEG responses time-lock at 80-90 Hz to continuous speech C_LIO_LIResponses primarily driven by high gamma rate fluctuations of the speech envelope C_LIO_LIResponse strength and latency are similar for younger and older adults C_LI

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Exaggerated Cortical Representation of Speech in Older Listeners: Mutual Information Analysis

Aging is associated with an exaggerated representation of the speech envelope in auditory cortex. The relationship between this age-related exaggerated response and a listeners ability to understand speech in noise remains an open question. Here, information-theory-based analysis methods are applied to magnetoencephalography (MEG) recordings of human listeners, investigating their cortical responses to continuous speech, using the novel non-linear measure of phase-locked mutual information between the speech stimuli and cortical responses. The cortex of older listeners shows an exaggerated level of mutual information, compared to younger listeners, for both attended and unattended speakers. The mutual information peaks for several distinct latencies: early ([~]50 ms), middle ([~]100 ms) and late ([~]200 ms). For the late component, the neural enhancement of attended over unattended speech is affected by stimulus SNR, but the direction of this dependency is reversed by aging. Critically, in older listeners and for the same late component, greater cortical exaggeration is correlated with decreased behavioral inhibitory control. This negative correlation also carries over to speech intelligibility in noise, where greater cortical exaggeration in older listeners is correlated with worse speech intelligibility scores. Finally, an age-related lateralization difference is also seen for the [~]100 ms latency peaks, where older listeners show a bilateral response compared to younger listeners right-lateralization. Thus, this information-theory-based analysis provides new, and less coarse-grained, results regarding age-related change in auditory cortical speech processing, and its correlation with cognitive measures, compared to related linear measures. New & NoteworthyCortical representations of natural speech are investigated using a novel non-linear approach based on mutual information. Cortical responses, phase-locked to the speech envelope, show an exaggerated level of mutual information associated with aging, appearing at several distinct latencies ([~]50, [~]100 and [~]200 ms). Critically, for older listeners only, the [~]200 ms latency response components are correlated with specific behavioral measures, including behavioral inhibition and speech comprehension.

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Mutual Information Analysis of Neural Representations of Speech in Noise in the Aging Midbrain

Younger adults with normal hearing can typically understand speech in the presence of a competing speaker without much effort, but this ability to understand speech in challenging conditions deteriorates with age. Older adults, even with clinically normal hearing, often have problems understanding speech in noise. Earlier auditory studies using the frequency-following response (FFR), primarily believed generated by the midbrain, have demonstrated age-related neural deficits when analyzed using traditional measures. Here we use a mutual information paradigm to analyze the FFR to speech (masked by a competing speech signal) by estimating the amount of stimulus information contained in the FFR. Our results show, first, a broad-band informational loss associated with aging for both FFR amplitude and phase. Second, this age-related loss of information is more severe in higher frequency FFR bands (several hundred Hz). Third, the mutual information between the FFR and the stimulus decreases as noise level increases for both age groups. Fourth, older adults benefit neurally, i.e., show a reduction in loss of information, when the speech masker is changed from meaningful (talker speaking a language that they can comprehend, such as English) to meaningless (talker speaking a language that they cannot comprehend, such as Dutch). This benefit is not seen in younger listeners, which suggests age-related informational loss may be more severe when the speech masker is meaningful than when it is meaningless. In summary, as a method, mutual information analysis can unveil new results that traditional measures may not have enough statistical power to assess.\n\nNew & NoteworthyOlder adults, even with clinically normal hearing, often have problems understanding speech in noise. Auditory studies using the frequency-following response (FFR) have demonstrated age-related neural deficits using traditional methods. Here we use a mutual information paradigm to analyze the FFR to speech masked by competing speech. Results confirm those using traditional analysis, but additionally show that older adults benefit neurally when the masker changes from a language that they comprehend to a language they cannot.

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Increased speech representation in older adults originates from early response in higher order auditory cortex

1Previous research has found that, paradoxically, while older adults have more difficulty comprehending speech in challenging circumstances than younger adults, their brain responses track the acoustic signal more robustly. Here we investigate this puzzle by using magnetoencephalography (MEG) source localization to determine the anatomical origin of this difference. Our results indicate that this robust tracking in older adults does not arise merely from having the same responses as younger adults but with larger amplitudes; instead they recruit additional regions, inferior to core auditory cortex, as part of an early response peak at ~ 30 ms relative to the acoustic signal.

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Representation of speech in noise in the aging midbrain and cortex: aging may dominate over hearing-loss

ObjectiveTo understand the effect of peripheral hearing loss on the representation of speech in noise in the aging midbrain and cortex.\n\nMethodsSubjects comprised 17 normal-hearing younger adults, 15 normal-hearing older adults and 14 hearing-impaired older adults. The midbrain response, measured with Frequency-Following Responses (FFRs), and the cortical response, measured with magnetoencephalography (MEG) responses, were recorded from subjects listening to speech in quiet and noise at varying signal to noise ratios (SNRs).\n\nResultsBoth groups of older listeners showed both weaker midbrain response amplitudes and overrepresentation of cortical responses compared to younger listeners. However, significant differences between the older groups were found in both midbrain-cortex relationships and in cortical processing durations, suggesting that hearing loss may alter reciprocal connections between lower and higher levels of the auditory pathway.\n\nConclusionsThe paucity of differences in midbrain or cortical responses between the two older groups suggest that age-related temporal processing deficits may contribute to older adults communication difficulties beyond what might be predicted from peripheral hearing loss alone.\n\nSignificanceClinical devices, such as hearing aids, should not ignore age-related temporal processing deficits in the design of algorithms to maximize user benefit.\n\nHIGHLIGHTSO_LIMild sensorineural hearing loss does not appear to significantly exacerbate already appreciable age-related deficits in midbrain speech-in-noise encoding.\nC_LIO_LIMild sensorineural hearing loss also does not appear to significantly exacerbate already appreciable age-related deficits in most measures of cortical speech-in-noise encoding.\nC_LIO_LICentral processing deficits caused by peripheral hearing loss in older adults are seen only in more subtle measures, including altered relationships between midbrain and cortex.\nC_LI

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Neural source dynamics of brain responses to continuous stimuli: speech processing from acoustics to comprehension

Human experience often involves continuous sensory information that unfolds over time. This is true in particular for speech comprehension, where continuous acoustic signals are processed over seconds or even minutes. We show that brain responses to such continuous stimuli can be investigated in detail, for magnetoencephalography (MEG) data by combining linear kernel estimation with minimum norm source localization. Previous research has shown that the requirement to average data over many trials can be overcome by modeling the brain response as a linear convolution of the stimulus and a kernel, or response function, and estimating a kernel that predicts the response from the stimulus. However, such analysis has been typically restricted to sensor space. Here we demonstrate that this analysis can also be performed in neural source space. We first computed distributed minimum norm current source estimates for continuous MEG recordings, and then computed response functions for the current estimate at each source element, using the boosting algorithm with cross-validation. Permutation tests can then assess the significance of individual predictor variables as well as features of the corresponding spatio-temporal response functions. We demonstrate the viability of this technique by computing spatio-temporal response functions for speech stimuli, using predictor variables reflecting acoustic, lexical and semantic processing. Results indicate that processes related to comprehension of continuous speech can be differentiated anatomically as well as temporally: acoustic information engaged auditory cortex at short latencies, followed by responses over the central sulcus and inferior frontal gyrus, possibly related to somatosensory/motor cortex involvement in speech perception; lexical frequency was associated with a left-lateralized response in auditory cortex and subsequent bilateral frontal activity; and semantic composition was associated with bilateral temporal and frontal brain activity. We conclude that this technique can be used to study the neural processing of continuous stimuli in time and anatomical space with the millisecond temporal resolution of MEG. This suggests new avenues for analyzing neural processing of naturalistic stimuli, without the necessity of averaging over artificially short or truncated stimuli.

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