Contributions of listening effort and intelligibility to cortical tracking of speech in adverse listening conditions.

Cortical tracking of speech is vital for speech segmentation and is linked to speech intelligibility. However, there is no clear consensus as to whether reduced intelligibility leads to a decrease or an increase in cortical speech tracking, warranting further investigation of the factors influencing this relationship. One such factor is listening effort, defined as the cognitive resources necessary for speech comprehension, and reported to have a strong negative correlation with speech intelligibility. Yet, no studies have examined the relationship between speech intelligibility, listening effort, and cortical tracking of speech. The aim of the present study was thus to examine these factors in quiet and distinct adverse listening conditions. Forty-nine normal hearing adults listened to sentences produced casually, presented in quiet and two adverse listening conditions: cafeteria noise and reverberant speech. Electrophysiological responses were registered with electroencephalogram, and listening effort was estimated subjectively using self-reported scores and objectively using pupillometry. Results indicated varying impacts of adverse conditions on intelligibility, listening effort, and cortical tracking of speech, depending on the preservation of the speech temporal envelope. The more distorted envelope in the reverberant condition led to higher listening effort, as reflected in higher subjective scores, increased pupil diameter, and stronger cortical tracking of speech in the delta band. These findings suggest that using measures of listening effort in addition to those of intelligibility is useful for interpreting cortical tracking of speech results. Moreover, reading and phonological skills of participants were positively correlated with listening effort in the cafeteria condition, suggesting a special role of expert language skills in processing speech in this noisy condition. Implications for future research and theories linking atypical cortical tracking of speech and reading disorders are further discussed.

Phonological deficits in dyslexia impede lexical processing of spoken words: Linking behavioural and MEG data.

Phonological difficulties have been identified as a core deficit in developmental dyslexia, yet everyday speech comprehension, which relies on phonological processing, is seemingly unaffected. This raises the question as to how dyslexic readers process spoken words to achieve normal word comprehension. Here we establish a link between neural correlates of lexical and sublexical processing in auditory words and behaviourally measured phonological deficits using magnetoencephalography (MEG). Spatiotemporally resolved cortical responses to phonological and lexico-semantic information were computed with the event-related regression technique (Hauk et al., 2009) and correlated with dyslexic and non-dyslexic subjects' phonological skills. We found that phonological deficits reduced cortical responses to both phonological and lexico-semantic information (phonological neighbours and word frequency). Individuals with lower phonological skills - independent of dyslexia diagnosis - showed weaker neural responses to phonological neighbourhood information in both hemispheres 200-500 ms after word onset and reduced sensitivity to written and spoken word frequency between 200 and 650 ms. Dyslexic readers showed weaker responses to written word frequency in particular compared to the control group, pointing towards an additional effect of print exposure on auditory word processing. Source space analysis localised phonological and lexico-semantic effect peaks to the left superior temporal gyrus, a key area that has been related to core deficits in dyslexia across a range of neuroimaging studies. The results provide comprehensive evidence that phonological deficits impact both sublexical and lexical stages of spoken word processing and that these deficits cannot be fully compensated through neural re-organization of lexical-distributional information at the single word level. Theoretical and practical implications for typical readers, dyslexic readers, and readers with developmental language disorder are discussed.

Theta-gamma phase-amplitude coupling in auditory cortex is modulated by language proficiency.

The coordination between the theta phase (3-7 Hz) and gamma power (25-35 Hz) oscillations (namely theta-gamma phase-amplitude coupling, PAC) in the auditory cortex has been proposed as an essential neural mechanism involved in speech processing. However, it has not been established how this mechanism is related to the efficiency with which a listener processes speech. Speech processing in a non-native language offers a useful opportunity to evaluate if theta-gamma PAC is modulated by the challenges imposed by the reception of speech input in a non-native language. The present study investigates how auditory theta-gamma PAC (recorded with magnetoencephalography) is modulated in both native and non-native speech reception. Participants were Spanish native (L1) speakers studying Basque (L2) at three different levels: beginner (Grade 1), intermediate (Grade 2), and advanced (Grade 3). We found that during L2 speech processing (i) theta-gamma PAC was more highly coordinated for intelligible compared to unintelligible speech; (ii) this coupling was modulated by proficiency in Basque being lower for beginners, higher for intermediate, and highest for advanced speakers (no difference observed in Spanish); (iii) gamma power did not differ between languages and groups. These findings highlight how the coordinated theta-gamma oscillatory activity is tightly related to speech comprehension: the stronger this coordination is, the more the comprehension system will proficiently parse the incoming speech input.

Temporal uncertainty enhances suppression of neural responses to predictable visual stimuli.

Contextual information triggers predictions about the content ("what") of environmental stimuli to update an internal generative model of the surrounding world. However, visual information dynamically changes across time, and temporal predictability ("when") may influence the impact of internal predictions on visual processing. In this magnetoencephalography (MEG) study, we investigated how processing feature specific information ("what") is affected by temporal predictability ("when"). Participants (N = 16) were presented with four consecutive Gabor patches (entrainers) with constant spatial frequency but with variable orientation and temporal onset. A fifth target Gabor was presented after a longer delay and with higher or lower spatial frequency that participants had to judge. We compared the neural responses to entrainers where the Gabor orientation could, or could not be temporally predicted along the entrainer sequence, and with inter-entrainer timing that was constant (predictable), or variable (unpredictable). We observed suppression of evoked neural responses in the visual cortex for predictable stimuli. Interestingly, we found that temporal uncertainty increased expectation suppression. This suggests that in temporally uncertain scenarios the neurocognitive system invests less resources in integrating bottom-up information. Multivariate pattern analysis showed that predictable visual features could be decoded from neural responses. Temporal uncertainty did not affect decoding accuracy for early visual responses, with the feature specificity of early visual neural activity preserved across conditions. However, decoding accuracy was less sustained over time for temporally jittered than for isochronous predictable visual stimuli. These findings converge to suggest that the cognitive system processes visual features of temporally predictable stimuli in higher detail, while processing temporally uncertain stimuli may rely more heavily on abstract internal expectations.

Reading-related brain changes in audiovisual processing: cross-sectional and longitudinal MEG evidence.

The ability to establish associations between visual objects and speech sounds is essential for human reading. Understanding the neural adjustments required for acquisition of these arbitrary audiovisual associations can shed light on fundamental reading mechanisms and help reveal how literacy builds on pre-existing brain circuits. To address these questions, the present longitudinal and cross-sectional MEG studies characterize the temporal and spatial neural correlates of audiovisual syllable congruency in children (4-9 years old, 22 males and 20 females) learning to read. Both studies showed that during the first years of reading instruction children gradually set up audiovisual correspondences between letters and speech sounds, which can be detected within the first 400 ms of a bimodal presentation and recruit the superior portions of the left temporal cortex. These findings suggest that children progressively change the way they treat audiovisual syllables as a function of their reading experience. This reading-specific brain plasticity implies (partial) recruitment of pre-existing brain circuits for audiovisual analysis.SIGNIFICANCE STATEMENTLinking visual and auditory linguistic representations is the basis for the development of efficient reading, while dysfunctional audiovisual letter processing predicts future reading disorders. Our developmental MEG project included a longitudinal and a cross-sectional study; both studies showed that children's audiovisual brain circuits progressively change as a function of reading experience. They also revealed an exceptional degree of neuroplasticity in audiovisual neural networks, showing that as children develop literacy, the brain progressively adapts so as to better detect new correspondences between letters and speech sounds.

Language Proficiency Entails Tuning Cortical Activity to Second Language Speech.

Cortical tracking of linguistic structures in speech, such as phrases (<3 Hz, delta band) and syllables (3-8 Hz, theta band), is known to be crucial for speech comprehension. However, it has not been established whether this effect is related to language proficiency. Here, we investigate how auditory cortical activity in second language (L2) learners tracked L2 speech. Using magnetoencephalography, we recorded brain activity from participants listening to Spanish and Basque. Participants were Spanish native (L1) language speakers studying Basque (L2) at the same language center at three different levels: beginner (Grade 1), intermediate (Grade 2), and advanced (Grade 3). We found that 1) both delta and theta tracking to L2 speech in the auditory cortex were related to L2 learning proficiency and that 2) top-down modulations of activity in the left auditory regions during L2 speech listening-by the left inferior frontal and motor regions in delta band and by the left middle temporal regions in theta band-were also related to L2 proficiency. Altogether, these results indicate that the ability to learn an L2 is related to successful cortical tracking of L2 speech and its modulation by neuronal oscillations in higher-order cortical regions.

Speech-brain phase coupling is enhanced in low contextual semantic predictability conditions.

Semantic prediction and cortical entrainment to the acoustic landmarks of the speech envelope are two fundamental yet qualitatively different mechanisms that facilitate speech comprehension. However, it is not clear how and to what extent those mechanisms interact with each other. On the one hand, richer semantic context could enhance the perceptual representation of a predictable stimulus, thus improving speech entrainment. On the other hand, pre-activating an upcoming item could inhibit further bottom-up analyses to minimize processing costs, thus weakening speech entrainment. To test these competing hypotheses, we recorded EEG activity from 27 participants while they listened to a 14-min recording of text reading. The passage contained target words presented twice: once in a highly constraining and once in a minimally constraining context. First, we measured event related potentials on target words in the two conditions. In line with previous research, we showed that semantic predictability modulated the N400 amplitude: words in minimally constraining contexts elicited larger negative amplitudes than words in highly constraining contexts between 250 and 450 ms. Second, we evaluated speech entrainment effects by analyzing phase alignment between neural activity and the envelope of target words. Importantly, we found increased speech entrainment for words in minimally constraining compared to highly constraining contexts between 400 and 450 ms. Both effects were located in central electrodes and were significantly correlated. Our results indicate a trade-off between semantic pre-activation and cortical entrainment to speech and support the cost minimization hypothesis.

Neural entrainment to speech and nonspeech in dyslexia: Conceptual replication and extension of previous investigations.

Whether phonological deficits in developmental dyslexia are associated with impaired neural sampling of auditory information is still under debate. Previous findings suggested that dyslexic participants showed atypical neural entrainment to slow and/or fast temporal modulations in speech, which might affect prosodic/syllabic and phonemic processing respectively. However, the large methodological variations across these studies do not allow us to draw clear conclusions on the nature of the entrainment deficit in dyslexia. Using magnetoencephalography, we measured neural entrainment to nonspeech and speech in both groups. We first aimed to conceptually replicate previous studies on auditory entrainment in dyslexia, using the same measurement methods as in previous studies, and also using new measurement methods (cross-correlation analyses) to better characterize the synchronization between stimulus and brain response. We failed to observe any of the significant group differences that had previously been reported in delta, theta and gamma frequency bands, whether using speech or nonspeech stimuli. However, when analyzing amplitude cross-correlations between noise stimuli and brain responses, we found that control participants showed larger responses than dyslexic participants in the delta range in the right hemisphere and in the gamma range in the left hemisphere. Overall, our results are weakly consistent with the hypothesis that dyslexic individuals show an atypical entrainment to temporal modulations. Our attempt at replicating previously published results highlights the multiple weaknesses of this research area, particularly low statistical power due to small sample size, and the lack of methodological standards inducing considerable heterogeneity of measurement and analysis methods across studies.

Impaired neural response to speech edges in dyslexia.

Speech comprehension has been proposed to critically rely on oscillatory cortical tracking, that is, phase alignment of neural oscillations to the slow temporal modulations (envelope) of speech. Speech-brain entrainment is readjusted over time as transient events (edges) in speech lead to speech-brain phase realignment. Auditory behavioral research suggests that phonological deficits in dyslexia are linked to difficulty in discriminating speech edges. Importantly, research to date has not specifically examined neural responses to speech edges in dyslexia. In the present study, we used MEG to record brain activity from normal and dyslexic readers while they listened to speech. We computed phase locking values (PLVs) to evaluate phase entrainment between neural oscillations and the speech envelope time-locked to edge onsets. In both groups, we observed that edge onsets induced phase resets in the auditory oscillations tracking speech, thereby enhancing their entrainment to speech. Importantly, dyslexic readers showed weaker PLVs compared to normal readers in left auditory regions from ~.15 sec to ~.65 sec after edge onset. Our results indicate that the neural mechanism that adapts cortical entrainment to the speech envelope is impaired in dyslexia. These findings here are consistent with the temporal sampling theory of developmental dyslexia.

Neocortical activity tracks the hierarchical linguistic structures of self-produced speech during reading aloud.

How the human brain uses self-generated auditory information during speech production is rather unsettled. Current theories of language production consider a feedback monitoring system that monitors the auditory consequences of speech output and an internal monitoring system, which makes predictions about the auditory consequences of speech before its production. To gain novel insights into underlying neural processes, we investigated the coupling between neuromagnetic activity and the temporal envelope of the heard speech sounds (i.e., cortical tracking of speech) in a group of adults who 1) read a text aloud, 2) listened to a recording of their own speech (i.e., playback), and 3) listened to another speech recording. Reading aloud was here used as a particular form of speech production that shares various processes with natural speech. During reading aloud, the reader's brain tracked the slow temporal fluctuations of the speech output. Specifically, auditory cortices tracked phrases (<1 â€‹Hz) but to a lesser extent than during the two speech listening conditions. Also, the tracking of words (2-4 â€‹Hz) and syllables (4-8 â€‹Hz) occurred at parietal opercula during reading aloud and at auditory cortices during listening. Directionality analyses were then used to get insights into the monitoring systems involved in the processing of self-generated auditory information. Analyses revealed that the cortical tracking of speech at <1 â€‹Hz, 2-4 â€‹Hz and 4-8 â€‹Hz is dominated by speech-to-brain directional coupling during both reading aloud and listening, i.e., the cortical tracking of speech during reading aloud mainly entails auditory feedback processing. Nevertheless, brain-to-speech directional coupling at 4-8 â€‹Hz was enhanced during reading aloud compared with listening, likely reflecting the establishment of predictions about the auditory consequences of speech before production. These data bring novel insights into how auditory verbal information is tracked by the human brain during perception and self-generation of connected speech.

Spatiotemporal dynamics of postoperative functional plasticity in patients with brain tumors in language areas.

Postoperative functional neuroimaging provides a unique opportunity to investigate the neural mechanisms that facilitate language network reorganization. Previous studies in patients with low grade gliomas (LGGs) in language areas suggest that postoperative recovery is likely due to functional neuroplasticity in peritumoral and contra-tumoral healthy regions, but have attributed varying degrees of importance to specific regions. In this study, we used Magnetoencephalography (MEG) to investigate functional connectivity changes in peritumoral and contra-tumoral regions after brain tumor resection. MEG recordings of cortical activity during resting-state were obtained from 12 patients with LGGs in left-hemisphere language brain areas. MEG data were recorded before (Pre session), and 3 (Post_1 session) and 6 (Post_2 session) months after awake craniotomy. For each MEG session, we measured the functional connectivity of the peritumoral and contra-tumoral regions to the rest of the brain across the 1-100 Hz frequency band. We found that functional connectivity in the Post_1 and Post_2 sessions was higher than in the Pre session only in peritumoral regions and within the alpha frequency band. Functional connectivity in peritumoral regions did not differ between the Post_1 and Post_2 sessions. Alpha connectivity enhancement in peritumoral regions was observed in all patients regardless of the LGG location. Together, these results suggest that postoperative language functional reorganization occurs in peritumoral regions regardless of the location of the tumor and mostly develops within 3 months after surgery.

Phase-amplitude coupling between theta and gamma oscillations adapts to speech rate.

Low- and high-frequency cortical oscillations play an important role in speech processing. Low-frequency neural oscillations in the delta (<4 Hz) and theta (4-8 Hz) bands entrain to the prosodic and syllabic rates of speech, respectively. Theta band neural oscillations modulate high-frequency neural oscillations in the gamma band (28-40 Hz), which have been hypothesized to be crucial for processing phonemes in natural speech. Since speech rate is known to vary considerably, both between and within talkers, it has yet to be determined whether this nested gamma response reflects an externally induced rhythm sensitive to the rate of the fine-grained structure of the input or a speech rate-independent endogenous response. Here, we recorded magnetoencephalography responses from participants listening to a speech delivered at different rates: decelerated, normal, and accelerated. We found that the phase of theta band oscillations in left and right auditory regions adjusts to speech rate variations. Importantly, we showed that the peak of the gamma response-coupled to the phase of theta-follows the speech rate. This indicates that gamma activity in auditory regions synchronizes with the fine-grain properties of speech, possibly reflecting detailed acoustic analysis of the input.

Delta(but not theta)-band cortical entrainment involves speech-specific processing.

Cortical oscillations phase-align to the quasi-rhythmic structure of the speech envelope. This speech-brain entrainment has been reported in two frequency bands, that is both in the theta band (4-8 Hz) and in the delta band (<4 Hz). However, it is not clear if these two phenomena reflect passive synchronization of the auditory cortex to the acoustics of the speech input, or if they reflect higher processes involved in actively parsing speech information. Here, we report two magnetoencephalography experiments in which we contrasted cortical entrainment to natural speech compared to qualitative different control conditions (Experiment 1: amplitude-modulated white-noise; Experiment 2: spectrally rotated speech). We computed the coherence between the oscillatory brain activity and the envelope of the auditory stimuli. At the sensor-level, we observed increased coherence for the delta and the theta band for all conditions in bilateral brain regions. However, only in the delta band (but not theta), speech entrainment was stronger than either of the control auditory inputs. Source reconstruction in the delta band showed that speech, compared to the control conditions, elicited larger coherence in the right superior temporal and left inferior frontal regions. In the theta band, no differential effects were observed for the speech compared to the control conditions. These results suggest that whereas theta entrainment mainly reflects perceptual processing of the auditory signal, delta entrainment involves additional higher-order computations in the service of language processing.

The Role of Slow Speech Amplitude Envelope for Speech Processing and Reading Development.

This study examined the putative link between the entrainment to the slow rhythmic structure of speech, speech intelligibility and reading by means of a behavioral paradigm. Two groups of 20 children (Grades 2 and 5) were asked to recall a pseudoword embedded in sentences presented either in quiet or noisy listening conditions. Half of the sentences were primed with their syllabic and prosodic amplitude envelope to determine whether a boost in auditory entrainment to these speech features enhanced pseudoword intelligibility. Priming improved pseudoword recall performance only for the older children both in a quiet and a noisy listening environment, and such benefit from the prime correlated with reading skills and pseudoword recall. Our results support the role of syllabic and prosodic tracking of speech in reading development.

Word and object recognition during reading acquisition: MEG evidence.

Studies on adults suggest that reading-induced brain changes might not be limited to linguistic processes. It is still unclear whether these results can be generalized to reading development. The present study shows to which extent neural responses to verbal and nonverbal stimuli are reorganized while children learn to read. MEG data of thirty Basque children (4-8y) were collected while they were presented with written words, spoken words and visual objects. The evoked fields elicited by the experimental stimuli were compared to their scrambled counterparts. Visual words elicited left posterior (200-300ms) and temporal activations (400-800ms). The size of these effects increased as reading performance improved, suggesting a reorganization of children's visual word responses. Spoken words elicited greater left temporal responses relative to scrambles (300-700ms). No evidence for the influence of reading expertise was observed. Brain responses to objects were greater than to scrambles in bilateral posterior regions (200-500ms). There was a greater left hemisphere involvement as reading errors decreased, suggesting a strengthened verbal decoding of visual configurations with reading acquisition. The present results reveal that learning to read not only influences written word processing, but also affects visual object recognition, suggesting a non-language specific impact of reading on children's neural mechanisms.

Out-of-synchrony speech entrainment in developmental dyslexia.

Developmental dyslexia is a reading disorder often characterized by reduced awareness of speech units. Whether the neural source of this phonological disorder in dyslexic readers results from the malfunctioning of the primary auditory system or damaged feedback communication between higher-order phonological regions (i.e., left inferior frontal regions) and the auditory cortex is still under dispute. Here we recorded magnetoencephalographic (MEG) signals from 20 dyslexic readers and 20 age-matched controls while they were listening to ∼10-s-long spoken sentences. Compared to controls, dyslexic readers had (1) an impaired neural entrainment to speech in the delta band (0.5-1 Hz); (2) a reduced delta synchronization in both the right auditory cortex and the left inferior frontal gyrus; and (3) an impaired feedforward functional coupling between neural oscillations in the right auditory cortex and the left inferior frontal regions. This shows that during speech listening, individuals with developmental dyslexia present reduced neural synchrony to low-frequency speech oscillations in primary auditory regions that hinders higher-order speech processing steps. The present findings, thus, strengthen proposals assuming that improper low-frequency acoustic entrainment affects speech sampling. This low speech-brain synchronization has the strong potential to cause severe consequences for both phonological and reading skills. Interestingly, the reduced speech-brain synchronization in dyslexic readers compared to normal readers (and its higher-order consequences across the speech processing network) appears preserved through the development from childhood to adulthood. Thus, the evaluation of speech-brain synchronization could possibly serve as a diagnostic tool for early detection of children at risk of dyslexia. Hum Brain Mapp 37:2767-2783, 2016. © 2016 Wiley Periodicals, Inc.

Developmental evaluation of atypical auditory sampling in dyslexia: Functional and structural evidence.

Whether phonological deficits in developmental dyslexia are associated with impaired neural sampling of auditory information at either syllabic- or phonemic-rates is still under debate. In addition, whereas neuroanatomical alterations in auditory regions have been documented in dyslexic readers, whether and how these structural anomalies are linked to auditory sampling and reading deficits remains poorly understood. In this study, we measured auditory neural synchronization at different frequencies corresponding to relevant phonological spectral components of speech in children and adults with and without dyslexia, using magnetoencephalography. Furthermore, structural MRI was used to estimate cortical thickness of the auditory cortex of participants. Dyslexics showed atypical brain synchronization at both syllabic (slow) and phonemic (fast) rates. Interestingly, while a left hemispheric asymmetry in cortical thickness was functionally related to a stronger left hemispheric lateralization of neural synchronization to stimuli presented at the phonemic rate in skilled readers, the same anatomical index in dyslexics was related to a stronger right hemispheric dominance for neural synchronization to syllabic-rate auditory stimuli. These data suggest that the acoustic sampling deficit in development dyslexia might be linked to an atypical specialization of the auditory cortex to both low and high frequency amplitude modulations.

Numbers are not like words: Different pathways for literacy and numeracy.

Literacy and numeracy are two fundamental cognitive skills that require mastering culturally-invented symbolic systems for representing spoken language and quantities. How numbers and words are processed in the human brain and their temporal dynamics remain unclear. Using MEG (magnetoencephalography), we find brain activation differences for literacy and numeracy from early stages of processing in the temporal-occipital and temporal-parietal regions. Native speakers of Spanish were exposed to visually presented words, pseudowords, strings of numbers, strings of letters and strings of symbols while engaged in a go/no-go task. Results showed more evoked neuromagnetic activity for words and pseudowords compared to symbols at ~120-130ms in the left occipito-temporal and temporal-parietal cortices (angular gyrus and intra-parietal sulcus) and at ~200ms in the left inferior frontal gyrus and left temporal areas. In contrast, numbers showed more activation than symbols at similar time windows in homologous regions of the right hemisphere: occipito-temporal and superior and middle temporal cortices at ~100-130ms. A direct comparison between the responses to words and numbers confirmed this distinct lateralization for the two stimulus types. These results suggest that literacy and numeracy follow distinct processing streams through the left and right hemispheres, respectively, and that the temporal-parietal and occipito-temporal regions may interact during processing alphanumeric stimuli.

Low frequency overactivation in dyslexia: Evidence from resting state Magnetoencephalography.

In this study, we compared the brain activation profiles obtained from resting state Magnetoencephalographic (MEG) activity in 15 dyslexic patients with the profiles of 15 normal controls, using power spectral density (PSD) analysis. We first estimated intracranial dipolar MEG sources on a dense grid on the cortical surface and then projected these sources on a standardized atlas with 68 regions of interest (ROIs). Averaging the PSD values of all sources in each ROI across all control subjects resulted in a normative database that was used to convert the PSD values of dyslexic patients into z-scores in eight distinct frequency bands. We found that dyslexic patients exhibited statistically significant overactivation in the delta band (0.1-4 Hz) in the right temporal (entorhinal and insula), left inferior frontal (Broca's area), and right inferior frontal regions. Overactivation may be interpreted as a compensatory mechanism for reading characterizing dyslexic patients. These findings suggest that resting-state MEG activation maps may be used as specific biomarkers that can help with the diagnosis of and assess the efficacy of intervention in dyslexia.