Comprehension of acoustically degraded speech in Alzheimer's disease and primary progressive aphasia

Successful communication in daily life depends on accurate decoding of speech signals that are acoustically degraded by challenging listening conditions. This process presents the brain with a demanding computational task that is vulnerable to neurodegenerative pathologies. However, despite recent intense interest in the link between hearing impairment and dementia, comprehension of acoustically degraded speech in these diseases has been little studied. Here we addressed this issue in a cohort of 19 patients with typical Alzheimer's disease and 30 patients representing the three canonical syndromes of primary progressive aphasia (nonfluent/agrammatic variant primary progressive aphasia; semantic variant primary progressive aphasia; logopenic variant primary progressive aphasia), compared to 25 healthy age-matched controls. As a paradigm for the acoustically degraded speech signals of daily life, we used noise-vocoding: synthetic division of the speech signal into frequency channels constituted from amplitude-modulated white noise, such that fewer channels convey less spectrotemporal detail thereby reducing intelligibility. We investigated the impact of noise-vocoding on recognition of spoken three-digit numbers and used psychometric modelling to ascertain the threshold number of noise-vocoding channels required for 50% intelligibility by each participant. Associations of noise-vocoded speech intelligibility threshold with general demographic, clinical and neuropsychological characteristics and regional grey matter volume (defined by voxel-based morphometry of patients' brain images) were also assessed. Mean noise-vocoded speech intelligibility threshold was significantly higher in all patient groups than healthy controls, and significantly higher in Alzheimer's disease and logopenic variant primary progressive aphasia than semantic variant primary progressive aphasia (all p < 0.05). In a receiver-operating-characteristic analysis, vocoded intelligibility threshold discriminated Alzheimer's disease, non-fluent variant and logopenic variant primary progressive aphasia patients very well from healthy controls. Further, this central hearing measure correlated with overall disease severity but not with peripheral hearing or clear speech perception. Neuroanatomically, after correcting for multiple voxel-wise comparisons in pre-defined regions of interest, impaired noise-vocoded speech comprehension across syndromes was significantly associated (p < 0.05) with atrophy of left planum temporale, angular gyrus and anterior cingulate gyrus: a cortical network that has previously been widely implicated in processing degraded speech signals. Our findings suggest that the comprehension of acoustically altered speech captures an auditory brain process relevant to daily hearing and communication in major dementia syndromes, with novel diagnostic and therapeutic implications

Responses in left inferior frontal gyrus are altered for speech‐in‐noise processing, but not for clear speech in autism

Introduction: Autistic individuals often have difficulties with recognizing what another person is saying in noisy conditions such as in a crowded classroom or a restaurant. The underlying neural mechanisms of this speech perception difficulty are unclear. In typically developed individuals, three cerebral cortex regions are particularly related to speech-in-noise perception: the left inferior frontal gyrus (IFG), the right insula, and the left inferior parietal lobule (IPL). Here, we tested whether responses in these cerebral cortex regions are altered in speech-in-noise perception in autism.Methods: Seventeen autistic adults and 17 typically developed controls (matched pairwise on age, sex, and IQ) performed an auditory-only speech recognition task during functional magnetic resonance imaging (fMRI). Speech was presented either with noise (noise condition) or without noise (no noise condition, i.e., clear speech).Results: In the left IFG, blood-oxygenation-level-dependent (BOLD) responses were higher in the control compared to the autism group for recognizing speech-in-noise compared to clear speech. For this contrast, both groups had similar response magnitudes in the right insula and left IPL. Additionally, we replicated previous findings that BOLD responses in speech-related and auditory brain regions (including bilateral superior temporal sulcus and Heschl's gyrus) for clear speech were similar in both groups and that voice identity recognition was impaired for clear and noisy speech in autism.Discussion: Our findings show that in autism, the processing of speech is particularly reduced under noisy conditions in the left IFG-a dysfunction that might be important in explaining restricted speech comprehension in noisy environments

Leading and following: Noise differently affects semantic and acoustic processing during naturalistic speech comprehension

Despite the distortion of speech signals caused by unavoidable noise in daily life, our ability to comprehend speech in noisy environments is relatively stable. However, the neural mechanisms underlying reliable speech-in-noise comprehension remain to be elucidated. The present study investigated the neural tracking of acoustic and semantic speech information during noisy naturalistic speech comprehension. Participants listened to narrative audio recordings mixed with spectrally matched stationary noise at three signal-to-ratio (SNR) levels (no noise, 3 dB, -3 dB), and 60-channel electroencephalography (EEG) signals were recorded. A temporal response function (TRF) method was employed to derive event-related-like responses to the continuous speech stream at both the acoustic and the semantic levels. Whereas the amplitude envelope of the naturalistic speech was taken as the acoustic feature, word entropy and word surprisal were extracted via the natural language processing method as two semantic features. Theta-band frontocentral TRF responses to the acoustic feature were observed at around 400 ms following speech fluctuation onset over all three SNR levels, and the response latencies were more delayed with increasing noise. Delta-band frontal TRF responses to the semantic feature of word entropy were observed at around 200 to 600 ms leading to speech fluctuation onset over all three SNR levels. The response latencies became more leading with increasing noise and decreasing speech comprehension and intelligibility. While the following responses to speech acoustics were consistent with previous studies, our study revealed the robustness of leading responses to speech semantics, which suggests a possible predictive mechanism at the semantic level for maintaining reliable speech comprehension in noisy environments

Predictive processing increases intelligibility of acoustically distorted speech : Behavioral and neural correlates

Introduction: We examined which brain areas are involved in the comprehension of acoustically distorted speech using an experimental paradigm where the same distorted sentence can be perceived at different levels of intelligibility. This change in intelligibility occurs via a single intervening presentation of the intact version of the sentence, and the effect lasts at least on the order of minutes. Since the acoustic structure of the distorted stimulus is kept fixed and only intelligibility is varied, this allows one to study brain activity related to speech comprehension specifically. Methods: In a functional magnetic resonance imaging (fMRI) experiment, a stimulus set contained a block of six distorted sentences. This was followed by the intact counterparts of the sentences, after which the sentences were presented in distorted form again. A total of 18 such sets were presented to 20 human subjects. Results: The blood oxygenation level dependent (BOLD)-responses elicited by the distorted sentences which came after the disambiguating, intact sentences were contrasted with the responses to the sentences presented before disambiguation. This revealed increased activity in the bilateral frontal pole, the dorsal anterior cingulate/paracingulate cortex, and the right frontal operculum. Decreased BOLD responses were observed in the posterior insula, Heschl's gyrus, and the posterior superior temporal sulcus. Conclusions: The brain areas that showed BOLD-enhancement for increased sentence comprehension have been associated with executive functions and with the mapping of incoming sensory information to representations stored in episodic memory. Thus, the comprehension of acoustically distorted speech may be associated with the engagement of memory-related subsystems. Further, activity in the primary auditory cortex was modulated by prior experience, possibly in a predictive coding framework. Our results suggest that memory biases the perception of ambiguous sensory information toward interpretations that have the highest probability to be correct based on previous experience.Peer reviewe

Pupil size tracks semantic ambiguity as well as noise

Effortful listening is experienced by listeners when speech is hard to understand because it is degraded or masked by environmental noise. Pupillometry (i.e., measure of pupil size) can detect effortful listening: pupil size increases when speech is degraded compared to when it is clear. However, the pupil responds to a range of cognitive demands, including linguistic challenges such as syntactic complexity. Here I investigate whether it responds to the need to disambiguate words with more than one meaning, such as ‘bark’ or ‘bank’. Semantic ambiguity is common in English, and previous work indicates that it imposes a processing load. We combine this with an acoustic challenge in a factorial design so the pupil response to these two types of challenge can be directly compared. I found main effects of noise and semantic ambiguity on the pupillary area, indicating that pupil dilation can reflect processes associated with semantic disambiguation as well as noise. Pupil size reflect demands imposed by ambiguity both in the acoustic form of words (i.e. due to degradation) and in word meaning

Cortical responses correlate with speech performance in pre-lingually deaf cochlear implant children

IntroductionCochlear implantation is currently the most successful intervention for severe-to-profound sensorineural hearing loss, particularly in deaf infants and children. Nonetheless, there remains a significant degree of variability in the outcomes of CI post-implantation. The purpose of this study was to understand the cortical correlates of the variability in speech outcomes with a cochlear implant in pre-lingually deaf children using functional near-infrared spectroscopy (fNIRS), an emerging brain-imaging technique.MethodsIn this experiment, cortical activities when processing visual speech and two levels of auditory speech, including auditory speech in quiet and in noise with signal-to-noise ratios of 10 dB, were examined in 38 CI recipients with pre-lingual deafness and 36 normally hearing children whose age and sex matched CI users. The HOPE corpus (a corpus of Mandarin sentences) was used to generate speech stimuli. The regions of interest (ROIs) for the fNIRS measurements were fronto-temporal-parietal networks involved in language processing, including bilateral superior temporal gyrus, left inferior frontal gyrus, and bilateral inferior parietal lobes.ResultsThe fNIRS results confirmed and extended findings previously reported in the neuroimaging literature. Firstly, cortical responses of superior temporal gyrus to both auditory and visual speech in CI users were directly correlated to auditory speech perception scores, with the strongest positive association between the levels of cross-modal reorganization and CI outcome. Secondly, compared to NH controls, CI users, particularly those with good speech perception, showed larger cortical activation in the left inferior frontal gyrus in response to all speech stimuli used in the experiment.DiscussionIn conclusion, cross-modal activation to visual speech in the auditory cortex of pre-lingually deaf CI children may be at least one of the neural bases of highly variable CI performance due to its beneficial effects for speech understanding, thus supporting the prediction and assessment of CI outcomes in clinic. Additionally, cortical activation of the left inferior frontal gyrus may be a cortical marker for effortful listening

Monolingual Versus Bilingual Use of Context to Facilitate Speech Recognition in Background Noise: A Systematic Review

Introduction: Previous literature has shown that bilingual listeners face more challenges than monolinguals during speech recognition in adverse listening conditions. As noisy environments degrade the acoustic stimuli and leave the listener with a partial or ambiguous signal to pair to a lexical representation, it is not possible to do so with the acoustic and phonological features alone. Bilinguals consistently use a significant amount of their cognitive resources during the early stages of speech processing, partially due to their need to navigate between the two languages. With exhaustion of most of their cognitive resources, there is limited capacity available to use higher-order processes, such as linguistic knowledge or semantic context in order to facilitate accurate recognition of the input signal when in noisy environments. The goal of this review was to determine the effect of linguistic background on the use of semantic context to enhance second language (L2), particularly English, speech recognition in adverse listening conditions. More specifically, this review examined the use of semantic context to enhance speech recognition by both bilinguals, with different Age of Acquisition (AoA), as well as monolinguals when listening in noise. Methods: 12 studies that investigated the use of semantic context to enhance speech recognition in monolingual and bilingual listeners were selected for this review. We were specifically interested in bilinguals with English as a L2. Results: Of the 12 studies included in this review, seven studies assessed monolinguals and bilinguals. Of these seven studies, five found that monolinguals were able to use semantic context clues better than bilinguals to facilitate accurate speech recognition in noisy environments. Most of the studies which pointed to poorer semantic context use in bilinguals evaluated subjects with later AoA. In addition, five of the 12 studies assessed the effects of AoA of the L2. Four of these studies determined that bilinguals with earlier AoA are better able to use semantic context to facilitate speech recognition in adverse listening conditions. Discussion and Conclusion: As the definition of bilinguals and bilingual subgroups vary according to different researchers, it is difficult to analyze the results without consideration for AoA. Analysis of our results suggest that bilingual use of semantic context is modulated by AoA. Most of the literature reviewed that points to poorer semantic context use in bilinguals compared to monolinguals used bilingual subjects with late AoA. Conclusion: It seems that the earlier the AoA, the better bilingual individuals are able to use semantic context to facilitate speech recognition in noisy environments

Decoding auditory attention and neural language processing in adverse conditions and different listener groups

This thesis investigated subjective, behavioural and neurophysiological (EEG) measures of speech processing in various adverse conditions and with different listener groups. In particular, this thesis focused on different neural processing stages and their relationship with auditory attention, effort, and measures of speech intelligibility. Study 1 set the groundwork by establishing a toolbox of various neural measures to investigate online speech processing, from the frequency following response (FFR) and cortical measures of speech processing, to the N400, a measure of lexico-semantic processing. Results showed that peripheral processing is heavily influenced by stimulus characteristics such as degradation, whereas central processing units are more closely linked to higher-order phenomena such as speech intelligibility. In Study 2, a similar experimental paradigm was used to investigate differences in neural processing between a hearing-impaired and a normal-hearing group. Subjects were presented with short stories in different levels of multi-talker babble noise, and with different settings on their hearing aids. Findings indicate that, particularly at lower noise levels, the hearing-impaired group showed much higher cortical entrainment than the normal- hearing group, despite similar levels of speech recognition. Intersubject correlation, another global neural measure of auditory attention, however, was similarly affected by noise levels in both the hearing-impaired and the normal-hearing group. This finding indicates extra processing in the hearing-impaired group only on the level of the auditory cortex. Study 3, in contrast to Studies 1 and 2 (which both investigated the effects of bottom-up factors on neural processing), examined the links between entrainment and top-down factors, specifically motivation; as well as reasons for the 5 higher entrainment found in hearing-impaired subjects in Study 2. Results indicated that, while behaviourally there was no difference between incentive and non-incentive conditions, neurophysiological measures of attention such as intersubject correlation were affected by the presence of an incentive to perform better. Moreover, using a specific degradation type resulted in subjects’ increased cortical entrainment under degraded conditions. These findings support the hypothesis that top-down factors such as motivation influence neurophysiological measures; and that higher entrainment to degraded speech might be triggered specifically by the reduced availability of spectral detail contained in speech

Finding the Means : The Bilingual Disparity in Semantic Context Use for Processing

Early and late bilinguals both differ in the speed with which they comprehend language or in their processing of sentences compared to monolinguals. This is possibly a result of crosslanguage interference, differential allocation of cognitive resources, or some other difference in language-dependent processes. This dissertation presents research and review focusing on one such language dependent process — the use of sentential context and lexical-associative semantic information — to process sentences. In a series of studies, 34 bilinguals and 28 monolinguals complete a retroactive masked priming task, which provides an isolated measure of the use of semantic information to backwards recognize degraded visual primes. Monolinguals demonstrated significantly faster reaction times as more semantic information became available in the conditions, whereas bilinguals did not. Compared to bilinguals, monolinguals also demonstrated faster reaction times in the condition of this task that had the most semantic information available to use for processing. These results suggest bilinguals use semantic information to activate word-level associates differently than monolinguals, and that their processing may even be inhibited by additional semantic context. Throughout this dissertation, these differential results are analyzed in the context of a differential processing mechanism in bilinguals and as the result of individual differences in cognition or their linguistic experiences

Investigating the relationship between cognitive control and speech-in-noise recognition in tinnitus from perceptual, neuroanatomical, and electrophysiological aspects

Purpose: Individuals with tinnitus commonly report difficulties understanding speech in adverse listening environments. Although such speech-in-noise (SiN) difficulties are believed to relate to deficits in cognitive control, there is as yet no evidence to underpin this assumption. The aim of this dissertation was to investigate the relationship between cognitive control and SiN recognition in individuals with tinnitus and normal hearing sensitivity. Method: Three studies linking behavioral to brain imaging measures were conducted. In the first study, the effect of tinnitus pitch on the recognition of consonants in noise at various frequency ranges was examined to better understand if the tinnitus percept impacts SiN recognition. Using voxel-based morphometry, the second study investigated the relationship between SiN performance and gray matter volume in auditory and cognitive processing regions in individuals with tinnitus. Lastly, using electroencephalogram to record brain activity during Go/Nogo tasks, the third study examined whether event-related potentials related to cognitive control are associated with SiN performance in individuals with tinnitus. Results and Discussion: Overall, the findings of the three studies suggest that 1) perceiving tinnitus at a given frequency does not interfere with speech recognition at the same frequency, suggesting that the effect of tinnitus on SiN recognition may involve higher-level cognitive processes rather than being solely mediated by perceptual abilities; 2) individuals with tinnitus and normal hearing showed comparable SiN recognition and neuropsychological performance relative to hearing-matched controls, however, they still demonstrated neuroanatomical changes and neural alterations pertaining to cognitive control; and 3) individuals with tinnitus may use different cognitive control strategies relative to hearing-matched controls to maintain their performance of daily tasks. Conclusions: The findings confirmed that incorporating multimodal approaches to examine the relationship between cognitive control and SiN recognition can be beneficial to detect neuroanatomical or neural alterations before any overt changes in behavioral performance. Further, the results will serve as the baseline for future endeavors to explicitly investigate the effect of tinnitus and hearing loss on cognitive control abilities and SiN recognition, which can be invaluable in advancing tinnitus consultation and intervention