Diminished Repetition Suppression Reveals Selective and Systems-Level Face Processing Differences in ASD.

Repeated exposure to a stimulus results in reduced neural response, or repetition suppression, in brain regions responsible for processing that stimulus. This rapid accommodation to repetition is thought to underlie learning, stimulus selectivity, and strengthening of perceptual expectations. Importantly, reduced sensitivity to repetition has been identified in several neurodevelopmental, learning, and psychiatric disorders, including autism spectrum disorder (ASD), a neurodevelopmental disorder characterized by challenges in social communication and repetitive behaviors and restricted interests. Reduced ability to exploit or learn from repetition in ASD is hypothesized to contribute to sensory hypersensitivities, and parallels several theoretical frameworks claiming that ASD individuals show difficulty using regularities in the environment to facilitate behavior. Using fMRI in autistic and neurotypical human adults (females and males), we assessed the status of repetition suppression across two modalities (vision, audition) and with four stimulus categories (faces, objects, printed words, and spoken words). ASD individuals showed domain-specific reductions in repetition suppression for face stimuli only, but not for objects, printed words, or spoken words. Reduced repetition suppression for faces was associated with greater challenges in social communication in ASD. We also found altered functional connectivity between atypically adapting cortical regions and higher-order face recognition regions, and microstructural differences in related white matter tracts in ASD. These results suggest that fundamental neural mechanisms and system-wide circuits are selectively altered for face processing in ASD and enhance our understanding of how disruptions in the formation of stable face representations may relate to higher-order social communication processes.SIGNIFICANCE STATEMENT A common finding in neuroscience is that repetition results in plasticity in stimulus-specific processing regions, reflecting selectivity and adaptation (repetition suppression [RS]). RS is reduced in several neurodevelopmental and psychiatric conditions including autism spectrum disorder (ASD). Theoretical frameworks of ASD posit that reduced adaptation may contribute to associated challenges in social communication and sensory processing. However, the scope of RS differences in ASD is unknown. We examined RS for multiple categories across visual and auditory domains (faces, objects, printed words, spoken words) in autistic and neurotypical individuals. We found reduced RS in ASD for face stimuli only and altered functional connectivity and white matter microstructure between cortical face-recognition areas. RS magnitude correlated with social communication challenges among autistic individuals.

Efficient functional localization of language regions in the brain.

Important recent advances in the cognitive neuroscience of language have been made using functional localizers to demarcate language-selective regions in individual brains. Although single-subject localizers offer insights that are unavailable in classic group analyses, they require additional scan time that imposes costs on investigators and participants. In particular, the unique practical challenges of scanning children and other special populations has led to less adoption of localizers for neuroimaging research with these theoretically and clinically important groups. Here, we examined how measurements of the spatial extent and functional response profiles of language regions are affected by the duration of an auditory language localizer. We compared how parametrically smaller amounts of data collected from one scanning session affected (i) consistency of group-level whole-brain parcellations, (ii) functional selectivity of subject-level activation in individually defined functional regions of interest (fROIs), (iii) sensitivity and specificity of subject-level whole-brain and fROI activation, and (iv) test-retest reliability of subject-level whole-brain and fROI activation. For many of these metrics, the localizer duration could be reduced by 50-75% while preserving the stability and reliability of both the spatial extent and functional response profiles of language areas. These results indicate that, for most measures relevant to cognitive neuroimaging studies, the brain's language network can be localized just as effectively with 3.5 min of scan time as it can with 12 min. Minimizing the time required to reliably localize the brain's language network allows more effective localizer use in situations where each minute of scan time is particularly precious.

Talker change detection by listeners varying in age and hearing loss.

Despite a vast literature on how speech intelligibility is affected by hearing loss and advanced age, remarkably little is known about the perception of talker-related information in these populations. Here, we assessed the ability of listeners to detect whether a change in talker occurred while listening to and identifying sentence-length sequences of words. Participants were recruited in four groups that differed in their age (younger/older) and hearing status (normal/impaired). The task was conducted in quiet or in a background of same-sex two-talker speech babble. We found that age and hearing loss had detrimental effects on talker change detection, in addition to their expected effects on word recognition. We also found subtle differences in the effects of age and hearing loss for trials in which the talker changed vs trials in which the talker did not change. These findings suggest that part of the difficulty encountered by older listeners, and by listeners with hearing loss, when communicating in group situations, may be due to a reduced ability to identify and discriminate between the participants in the conversation.

Both stronger and weaker cerebro-cerebellar functional connectivity patterns during processing of spoken sentences in autism spectrum disorder.

Cerebellar differences have long been documented in autism spectrum disorder (ASD), yet the extent to which such differences might impact language processing in ASD remains unknown. To investigate this, we recorded brain activity with magnetoencephalography (MEG) while ASD and age-matched typically developing (TD) children passively processed spoken meaningful English and meaningless Jabberwocky sentences. Using a novel source localization approach that allows higher resolution MEG source localization of cerebellar activity, we found that, unlike TD children, ASD children showed no difference between evoked responses to meaningful versus meaningless sentences in right cerebellar lobule VI. ASD children also had atypically weak functional connectivity in the meaningful versus meaningless speech condition between right cerebellar lobule VI and several left-hemisphere sensorimotor and language regions in later time windows. In contrast, ASD children had atypically strong functional connectivity for in the meaningful versus meaningless speech condition between right cerebellar lobule VI and primary auditory cortical areas in an earlier time window. The atypical functional connectivity patterns in ASD correlated with ASD severity and the ability to inhibit involuntary attention. These findings align with a model where cerebro-cerebellar speech processing mechanisms in ASD are impacted by aberrant stimulus-driven attention, which could result from atypical temporal information and predictions of auditory sensory events by right cerebellar lobule VI.

Multiple sources of acoustic variation affect speech processing efficiency.

Phonetic variability across talkers imposes additional processing costs during speech perception, evident in performance decrements when listening to speech from multiple talkers. However, within-talker phonetic variation is a less well-understood source of variability in speech, and it is unknown how processing costs from within-talker variation compare to those from between-talker variation. Here, listeners performed a speeded word identification task in which three dimensions of variability were factorially manipulated: between-talker variability (single vs multiple talkers), within-talker variability (single vs multiple acoustically distinct recordings per word), and word-choice variability (two- vs six-word choices). All three sources of variability led to reduced speech processing efficiency. Between-talker variability affected both word-identification accuracy and response time, but within-talker variability affected only response time. Furthermore, between-talker variability, but not within-talker variability, had a greater impact when the target phonological contrasts were more similar. Together, these results suggest that natural between- and within-talker variability reflect two distinct magnitudes of common acoustic-phonetic variability: Both affect speech processing efficiency, but they appear to have qualitatively and quantitatively unique effects due to differences in their potential to obscure acoustic-phonemic correspondences across utterances.

Energetic and informational masking place dissociable demands on listening effort: Evidence from simultaneous electroencephalography and pupillometrya).

The task of processing speech masked by concurrent speech/noise can pose a substantial challenge to listeners. However, performance on such tasks may not directly reflect the amount of listening effort they elicit. Changes in pupil size and neural oscillatory power in the alpha range (8-12 Hz) are prominent neurophysiological signals known to reflect listening effort; however, measurements obtained through these two approaches are rarely correlated, suggesting that they may respond differently depending on the specific cognitive demands (and, by extension, the specific type of effort) elicited by specific tasks. This study aimed to compare changes in pupil size and alpha power elicited by different types of auditory maskers (highly confusable intelligible speech maskers, speech-envelope-modulated speech-shaped noise, and unmodulated speech-shaped noise maskers) in young, normal-hearing listeners. Within each condition, the target-to-masker ratio was set at the participant's individually estimated 75% correct point on the psychometric function. The speech masking condition elicited a significantly greater increase in pupil size than either of the noise masking conditions, whereas the unmodulated noise masking condition elicited a significantly greater increase in alpha oscillatory power than the speech masking condition, suggesting that the effort needed to solve these respective tasks may have different neural origins.

Common cortical architectures for phonological working memory identified in individual brains.

Phonological working memory is the capacity to briefly maintain and recall representations of sounds important for speech and language and is believed to be critical for language and reading acquisition. Whether phonological working memory is supported by fronto-parietal brain regions associated with short-term memory storage or perisylvian brain structures implicated in speech perception and production is unclear, perhaps due to variability in stimuli, task demands, and individuals. We used fMRI to assess neurophysiological responses while individuals performed two tasks with closely matched stimuli but divergent task demands-nonword repetition and nonword discrimination-at two levels of phonological working memory load. Using analyses designed to address intersubject variability, we found significant neural responses to the critical contrast of high vs. low phonological working memory load in both tasks in a set of regions closely resembling those involved in speech perception and production. Moreover, within those regions, the voxel-wise patterns of load-related activation were highly correlated between the two tasks. These results suggest that brain regions in the temporal and frontal lobes encapsulate the core neurocomputational components of phonological working memory; an architecture that becomes increasingly evident as neural responses are examined in successively finer-grained detail in individual participants.

Speech processing and plasticity in the right hemisphere predict variation in adult foreign language learning.

Foreign language learning in adulthood often takes place in classrooms where learning outcomes vary widely among students, for both initial learning and long-term retention. Despite the fundamental role of speech perception in first language acquisition, its role in foreign language learning outcomes remains unknown. Using a speech discrimination functional magnetic resonance imaging (fMRI) task and resting-state fMRI before and after an intensive, classroom-based, Mandarin Chinese course, we examined how variations in pre-training organization and pre-to-post reorganization of brain functions predicted successful language learning in male and female native English-speakers. Greater pre-training activation in right inferior frontal gyrus (IFG) to Mandarin speech was associated with better Mandarin attainment at the end of the course. After four weeks of class, learners showed overall increased activation in left IFG and left superior parietal lobule (SPL) to Mandarin speech, but in neither region was variation related to learning outcomes. Immediate attainment was associated with greater pre-to-post reduction of right IFG activation to Mandarin speech but also greater enhancement of resting-state connectivity between this region and both left IFG and left SPL. Long-term retention of Mandarin skills measured three months later was more accurately predicted by models using features of neural preparedness (pre-training activation) and neural plasticity (pre-to-post activation change) than models using behavior preparedness and plasticity features (pre-training speech discrimination accuracy and Mandarin attainment, respectively). These findings suggest that successful holistic foreign language acquisition in human adulthood requires right IFG engagement during initial learning but right IFG disengagement for long-term retention of language skills.

Acoustic and linguistic factors affecting perceptual dissimilarity judgments of voices.

The human voice is a complex acoustic signal that conveys talker identity via individual differences in numerous features, including vocal source acoustics, vocal tract resonances, and dynamic articulations during speech. It remains poorly understood how differences in these features contribute to perceptual dissimilarity of voices and, moreover, whether linguistic differences between listeners and talkers interact during perceptual judgments of voices. Here, native English- and Mandarin-speaking listeners rated the perceptual dissimilarity of voices speaking English or Mandarin from either forward or time-reversed speech. The language spoken by talkers, but not listeners, principally influenced perceptual judgments of voices. Perceptual dissimilarity judgments of voices were always highly correlated between listener groups and forward/time-reversed speech. Representational similarity analyses that explored how acoustic features (fundamental frequency mean and variation, jitter, harmonics-to-noise ratio, speech rate, and formant dispersion) contributed to listeners' perceptual dissimilarity judgments, including how talker- and listener-language affected these relationships, found the largest effects relating to voice pitch. Overall, these data suggest that, while linguistic factors may influence perceptual judgments of voices, the magnitude of such effects tends to be very small. Perceptual judgments of voices by listeners of different native language backgrounds tend to be more alike than different.

Talker identification: Effects of masking, hearing loss, and age.

The ability to identify who is talking is an important aspect of communication in social situations and, while empirical data are limited, it is possible that a disruption to this ability contributes to the difficulties experienced by listeners with hearing loss. In this study, talker identification was examined under both quiet and masked conditions. Subjects were grouped by hearing status (normal hearing/sensorineural hearing loss) and age (younger/older adults). Listeners first learned to identify the voices of four same-sex talkers in quiet, and then talker identification was assessed (1) in quiet, (2) in speech-shaped, steady-state noise, and (3) in the presence of a single, unfamiliar same-sex talker. Both younger and older adults with hearing loss, as well as older adults with normal hearing, generally performed more poorly than younger adults with normal hearing, although large individual differences were observed in all conditions. Regression analyses indicated that both age and hearing loss were predictors of performance in quiet, and there was some evidence for an additional contribution of hearing loss in the presence of masking. These findings suggest that both hearing loss and age may affect the ability to identify talkers in "cocktail party" situations.

Foreign language talker identification does not generalize to new talkers.

Listeners identify talkers less accurately in a foreign language than in their native language, but it remains unclear whether this language-familiarity effect arises because listeners (1) simply lack experience identifying foreign-language talkers or (2) gain access to additional talker-specific information during concurrent linguistic processing of talkers' speech. Here, we tested whether sustained practice identifying talkers of an unfamiliar, foreign language could lead to generalizable improvement in learning to identify new talkers speaking that language, even if listeners remained unable to understand the talkers' speech. English-speaking adults with no prior experience with Mandarin practiced learning to identify Mandarin-speaking talkers over four consecutive days and were tested on their ability to generalize their Mandarin talker-identification abilities to new Mandarin-speaking talkers on the fourth day. In a "same-voices" training condition, listeners learned to identify the same talkers for the first 3 days and new talkers on the fourth day; in a "different-voices" condition, listeners learned to identify a different set of voices on each day including the fourth day. Listeners in the same-voices condition showed daily improvement in talker identification across the first 3 days but returned to baseline when trying to learn new talkers on the fourth day, whereas listeners in the different-voices condition showed no improvement across the 4 days. After 4 days, neither group demonstrated generalized improvement in learning new Mandarin-speaking talkers versus their baseline performance. These results suggest that, in the absence of specific linguistic knowledge, listeners are unable to develop generalizable foreign-language talker-identification abilities.

Musical training does not enhance neural sound encoding at early stages of the auditory system: A large-scale multisite investigation.

Musical training has been associated with enhanced neural processing of sounds, as measured via the frequency following response (FFR), implying the potential for human subcortical neural plasticity. We conducted a large-scale multi-site preregistered study (n > 260) to replicate and extend the findings underpinning this important relationship. We failed to replicate any of the major findings published previously in smaller studies. Musical training was related neither to enhanced spectral encoding strength of a speech stimulus (/da/) in babble nor to a stronger neural-stimulus correlation. Similarly, the strength of neural tracking of a speech sound with a time-varying pitch was not related to either years of musical training or age of onset of musical training. Our findings provide no evidence for plasticity of early auditory responses based on musical training and exposure.

Atypical cortical processing of bottom-up speech binding cues in children with autism spectrum disorders.

Individuals with autism spectrum disorder (ASD) commonly display speech processing abnormalities. Binding of acoustic features of speech distributed across different frequencies into coherent speech objects is fundamental in speech perception. Here, we tested the hypothesis that the cortical processing of bottom-up acoustic cues for speech binding may be anomalous in ASD. We recorded magnetoencephalography while ASD children (ages 7-17) and typically developing peers heard sentences of sine-wave speech (SWS) and modulated SWS (MSS) where binding cues were restored through increased temporal coherence of the acoustic components and the introduction of harmonicity. The ASD group showed increased long-range feedforward functional connectivity from left auditory to parietal cortex with concurrent decreased local functional connectivity within the parietal region during MSS relative to SWS. As the parietal region has been implicated in auditory object binding, our findings support our hypothesis of atypical bottom-up speech binding in ASD. Furthermore, the long-range functional connectivity correlated with behaviorally measured auditory processing abnormalities, confirming the relevance of these atypical cortical signatures to the ASD phenotype. Lastly, the group difference in the local functional connectivity was driven by the youngest participants, suggesting that impaired speech binding in ASD might be ameliorated upon entering adolescence.

Altered engagement of the speech motor network is associated with reduced phonological working memory in autism.

Nonword repetition, a common clinical measure of phonological working memory, involves component processes of speech perception, working memory, and speech production. Autistic children often show behavioral challenges in nonword repetition, as do many individuals with communication disorders. It is unknown which subprocesses of phonological working memory are vulnerable in autistic individuals, and whether the same brain processes underlie the transdiagnostic difficulty with nonword repetition. We used functional magnetic resonance imaging (fMRI) to investigate the brain bases for nonword repetition challenges in autism. We compared activation during nonword repetition in functional brain networks subserving speech perception, working memory, and speech production between neurotypical and autistic children. Autistic children performed worse than neurotypical children on nonword repetition and had reduced activation in response to increasing phonological working memory load in the supplementary motor area. Multivoxel pattern analysis within the speech production network classified shorter vs longer nonword-repetition trials less accurately for autistic than neurotypical children. These speech production motor-specific differences were not observed in a group of children with reading disability who had similarly reduced nonword repetition behavior. These findings suggest that atypical function in speech production brain regions may contribute to nonword repetition difficulties in autism.

Implicit and explicit learning in talker identification.

In the real world, listeners seem to implicitly learn talkers' vocal identities during interactions that prioritize attending to the content of talkers' speech. In contrast, most laboratory experiments of talker identification employ training paradigms that require listeners to explicitly practice identifying voices. Here, we investigated whether listeners become familiar with talkers' vocal identities during initial exposures that do not involve explicit talker identification. Participants were assigned to one of three exposure tasks, in which they heard identical stimuli but were differentially required to attend to the talkers' vocal identity or to the verbal content of their speech: (1) matching the talker to a concurrent visual cue (talker-matching); (2) discriminating whether the talker was the same as the prior trial (talker 1-back); or (3) discriminating whether speech content matched the previous trial (verbal 1-back). All participants were then tested on their ability to learn to identify talkers from novel speech content. Critically, we manipulated whether the talkers during this post-test differed from those heard during training. Compared to learning to identify novel talkers, listeners were significantly more accurate learning to identify the talkers they had previously been exposed to in the talker-matching and verbal 1-back tasks, but not the talker 1-back task. The correlation between talker identification test performance and exposure task performance was also greater when the talkers were the same in both tasks. These results suggest that listeners learn talkers' vocal identity implicitly during speech perception, even if they are not explicitly attending to the talkers' identity.

Distinct mechanisms for talker adaptation operate in parallel on different timescales.

The mapping between speech acoustics and phonemic representations is highly variable across talkers, and listeners are slower to recognize words when listening to multiple talkers compared with a single talker. Listeners' speech processing efficiency in mixed-talker settings improves when given time to reorient their attention to each new talker. However, it remains unknown how much time is needed to fully reorient attention to a new talker in mixed-talker settings so that speech processing becomes as efficient as when listening to a single talker. In this study, we examined how speech processing efficiency improves in mixed-talker settings as a function of the duration of continuous speech from a talker. In single-talker and mixed-talker conditions, listeners identified target words either in isolation or preceded by a carrier vowel of parametrically varying durations from 300 to 1,500 ms. Listeners' word identification was significantly slower in every mixed-talker condition compared with the corresponding single-talker condition. The costs associated with processing mixed-talker speech declined significantly as the duration of the speech carrier increased from 0 to 600 ms. However, increasing the carrier duration beyond 600 ms did not achieve further reduction in talker variability-related processing costs. These results suggest that two parallel mechanisms support processing talker variability: A stimulus-driven mechanism that operates on short timescales to reorient attention to new auditory sources, and a top-down mechanism that operates over longer timescales to allocate the cognitive resources needed to accommodate uncertainty in acoustic-phonemic correspondences during contexts where speech may come from multiple talkers.

Socioeconomic dissociations in the neural and cognitive bases of reading disorders.

Childhood socioeconomic status (SES) strongly predicts disparities in reading development, yet it is unknown whether early environments also moderate the cognitive and neurobiological bases of reading disorders (RD) such as dyslexia, the most prevalent learning disability. SES-diverse 6-9-year-old children (n = 155, half with RD) completed behavioral and functional magnetic resonance imaging (fMRI) tasks engaging phonological and orthographic processing, which revealed corresponding double-dissociations in neurocognitive deficits. At the higher end of the SES spectrum, RD was most strongly explained by differences in phonological skill and corresponding activation in left inferior frontal and temporoparietal regions during phonological processing-widely considered the "core deficit" of RD. However, at the lower end of the SES spectrum, RD was most strongly explained by differences in rapid naming skills and corresponding activation in left temporoparietal and fusiform regions during orthographic processing. Findings indicate that children's early environments systematically moderate the neurocognitive systems underlying RD, which has implications for assessment and treatment approaches to reduce SES disparities in RD outcomes. Further, results suggest that reliance on high-SES convenience samples may mask critical heterogeneity in the foundations of both typical and disordered reading development.

The Neural Representation of a Repeated Standard Stimulus in Dyslexia.

The neural representation of a repeated stimulus is the standard against which a deviant stimulus is measured in the brain, giving rise to the well-known mismatch response. It has been suggested that individuals with dyslexia have poor implicit memory for recently repeated stimuli, such as the train of standards in an oddball paradigm. Here, we examined how the neural representation of a standard emerges over repetitions, asking whether there is less sensitivity to repetition and/or less accrual of "standardness" over successive repetitions in dyslexia. We recorded magnetoencephalography (MEG) as adults with and without dyslexia were passively exposed to speech syllables in a roving-oddball design. We performed time-resolved multivariate decoding of the MEG sensor data to identify the neural signature of standard vs. deviant trials, independent of stimulus differences. This "multivariate mismatch" was equally robust and had a similar time course in the two groups. In both groups, standards generated by as few as two repetitions were distinct from deviants, indicating normal sensitivity to repetition in dyslexia. However, only in the control group did standards become increasingly different from deviants with repetition. These results suggest that many of the mechanisms that give rise to neural adaptation as well as mismatch responses are intact in dyslexia, with the possible exception of a putatively predictive mechanism that successively integrates recent sensory information into feedforward processing.

Electrophysiological correlates of perceptual prediction error are attenuated in dyslexia.

A perceptual adaptation deficit often accompanies reading difficulty in dyslexia, manifesting in poor perceptual learning of consistent stimuli and reduced neurophysiological adaptation to stimulus repetition. However, it is not known how adaptation deficits relate to differences in feedforward or feedback processes in the brain. Here we used electroencephalography (EEG) to interrogate the feedforward and feedback contributions to neural adaptation as adults with and without dyslexia viewed pairs of faces and words in a paradigm that manipulated whether there was a high probability of stimulus repetition versus a high probability of stimulus change. We measured three neural dependent variables: expectation (the difference between prestimulus EEG power with and without the expectation of stimulus repetition), feedforward repetition (the difference between event-related potentials (ERPs) evoked by an expected change and an unexpected repetition), and feedback-mediated prediction error (the difference between ERPs evoked by an unexpected change and an expected repetition). Expectation significantly modulated prestimulus theta- and alpha-band EEG in both groups. Unexpected repetitions of words, but not faces, also led to significant feedforward repetition effects in the ERPs of both groups. However, neural prediction error when an unexpected change occurred instead of an expected repetition was significantly weaker in dyslexia than the control group for both faces and words. These results suggest that the neural and perceptual adaptation deficits observed in dyslexia reflect the failure to effectively integrate perceptual predictions with feedforward sensory processing. In addition to reducing perceptual efficiency, the attenuation of neural prediction error signals would also be deleterious to the wide range of perceptual and procedural learning abilities that are critical for developing accurate and fluent reading skills.

Speech-specific perceptual adaptation deficits in children and adults with dyslexia.

According to several influential theoretical frameworks, phonological deficits in dyslexia result from reduced sensitivity to acoustic cues that are essential for the development of robust phonemic representations. Some accounts suggest that these deficits arise from impairments in rapid auditory adaptation processes that are either speech-specific or domain-general. Here, we examined the specificity of auditory adaptation deficits in dyslexia using a nonlinguistic tone anchoring (adaptation) task and a linguistic selective adaptation task in children and adults with and without dyslexia. Children and adults with dyslexia had elevated tone-frequency discrimination thresholds, but both groups benefited from anchoring to repeated stimuli to the same extent as typical readers. Additionally, although both dyslexia groups had overall reduced accuracy for speech sound identification, only the child group had reduced categorical perception for speech. Across both age groups, individuals with dyslexia had reduced perceptual adaptation to speech. These results highlight broad auditory perceptual deficits across development in individuals with dyslexia for both linguistic and nonlinguistic domains, but speech-specific adaptation deficits. Finally, mediation models in children and adults revealed that the causal pathways from basic perception and adaptation to phonological awareness through speech categorization were not significant. Thus, rather than having causal effects, perceptual deficits may co-occur with the phonological deficits in dyslexia across development. (PsycInfo Database Record (c) 2022 APA, all rights reserved).