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Johnsrude, I. S.

Publications and source records attributed to Johnsrude, I. S..

17 recordsLinked to original sources

Prediction from Statistical Learning Aids Auditory Scene Analysis

Statistical regularities support auditory scene analysis across multiple levels. While acoustic regularities like comodulation and harmonicity aid bottom-up perceptual grouping, higher-level regularities like linguistic or musical structure must be learned to form a mental "schema" of statistical patterns. Although learned schemas may benefit comprehension by helping listeners perceptually separate and/or attend to a target sound stream in an acoustic mixture, the underlying mechanisms are unclear. Here, we used a statistical learning paradigm to expose listeners to sequences of speech syllables with fixed transitional probabilities, forming an artificial "language" of trisyllabic words. Following exposure, participants attended to one of two concurrent syllable streams and detected target syllables. Detection performance improved when the attended stream conformed to the statistical structure learned implicitly during exposure, with a larger benefit in the presence of a competing stream than in quiet. In contrast, predictability of the unattended stream had no effect on performance. Electroencephalography revealed that predictable targets elicited earlier parietal P300 "target-recognition" responses and enhanced neural tracking of the attended stream, with additional signatures of predictive processing observed even in the absence of targets. These findings demonstrate that learned statistical regularities enhance listening in noise by enabling predictive, schema-based selection of relevant input. Rather than facilitating automatic segregation of competing sounds, learned lexical schemas support auditory scene analysis through attentional template matching. Our findings establish a direct mechanistic link to the role of prediction in schema-based listening in noise. SignificanceOur remarkable ability to isolate a target sound source, such as a persons voice, in noisy environments is essential for effective communication. This process--termed auditory scene analysis--is known to rely on low-level acoustic regularities, but it is unclear whether learned higher-level regularities, like linguistic structure, also contribute. Combined electroencephalography and behavioral experiments reveal that statistical prediction of upcoming target syllables based on learned syllable-transition probabilities of an artificial language improves attentional selection to a target sound stream in an acoustic mixture. Prediction enhances neural tracking of the attended stream and speeds neural recognition of auditory targets. These findings have implications for auditory training approaches to rehabilitate hearing-impaired individuals who struggle to understand speech in noise.

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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.

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The Effects of Speech Masking on Neural Tracking of Acoustic and Semantic Features of Natural Speech

Listening environments contain background sounds that mask speech and lead to communication challenges. Sensitivity to slow acoustic fluctuations in speech can help segregate speech from background noise. Semantic context can also facilitate speech perception in noise, for example, by enabling prediction of upcoming words. However, not much is known about how different degrees of background masking affect the neural processing of acoustic and semantic features during naturalistic speech listening. In the current electroencephalography (EEG) study, participants listened to engaging, spoken stories masked at different levels of multi-talker babble to investigate how neural activity in response to acoustic and semantic features changes with acoustic challenges, and how such effects relate to speech intelligibility. The pattern of neural response amplitudes associated with both acoustic and semantic speech features across masking levels was U-shaped, such that amplitudes were largest for moderate masking levels. This U-shape may be due to increased attentional focus when speech comprehension is challenging, but manageable. The latency of the neural responses increased linearly with increasing background masking, and neural latency change associated with acoustic processing most closely mirrored the changes in speech intelligibility. Finally, tracking responses related to semantic dissimilarity remained robust until severe speech masking (-3 dB SNR). The current study reveals that neural responses to acoustic features are highly sensitive to background masking and decreasing speech intelligibility, whereas neural responses to semantic features are relatively robust, suggesting that individuals track the meaning of the story well even in moderate background sound.

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Age-related changes in neural synchronization and the sustained response to amplitude and frequency modulation of sound

Perception of speech requires sensitivity to features, such as amplitude and frequency modulations, that are often temporally regular. Previous work suggests age-related changes in neural responses to temporally regular features, but little work has focused on age differences for different types of modulations. We recorded magnetoencephalography in younger (21-33 years) and older adults (53-73 years) to investigate age differences in neural responses to slow (2-6 Hz sinusoidal and non-sinusoidal) modulations in amplitude, frequency, or combined amplitude and frequency. Audiometric pure-tone average thresholds were elevated in older compared to younger adults, indicating subclinical hearing impairment in the recruited older-adult sample. Neural responses to sound onset (independent of temporal modulations) were increased in magnitude in older compared to younger adults, suggesting hyperresponsivity and a loss of inhibition in the aged auditory system. Analyses of neural activity to modulations revealed greater neural synchronization with amplitude, frequency, and combined amplitude-frequency modulations for older compared to younger adults. This potentiated response generalized across different degrees of temporal regularity (sinusoidal and non-sinusoidal), although neural synchronization was generally lower for non-sinusoidal modulation. Despite greater synchronization, sustained neural activity was reduced in older compared to younger adults for sounds modulated both sinusoidally and non-sinusoidally in frequency. Our results suggest age differences in the sensitivity of the auditory system to features present in speech and other natural sounds.

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Age-related changes in the neural mechanics of dynamic auditory attention in time

Listening in everyday life requires attention to be deployed dynamically - when listening is expected to be difficult and when relevant information is expected to occur - to conserve mental resources. Conserving mental resources may be particularly important for older adults who often experience difficulties understanding speech. In the current study, we use electro- and magnetoencephalography to investigate the neural and behavioral mechanics of attention regulation during listening and the effects that aging has on these. We show that neural alpha oscillatory activity indicates when in time attention is deployed (Experiment 1) and that deployment depends on listening difficulty (Experiment 2). Older adults (54-72 years) also show successful attention regulation but appear to utilize timing information differently compared to younger adults (20-33 years). We further show a notable age-group dissociation in recruited brain regions. In younger adults, superior parietal cortex underlies alpha power during attention regulation, whereas, in older adults, alpha power emerges from more ventro-lateral areas (posterior temporal cortex; Experiment 3). This difference in the sources of alpha activity between age groups only occurred during task performance and was absent during rest (Experiment S1). In sum, our study suggests that older adults employ different neural control strategies compared to younger adults to regulate attention in time under listening challenges.

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Neural activity in human brainstem adapts to sound-level statistics

Optimal perception requires adaptation to sounds in the environment. Adaptation involves representing the acoustic stimulation history in neural response patterns, for example, by altering response magnitude or latency as sound-level context change. Neurons in the auditory brainstem of rodents are sensitive to acoustic stimulation history and sound-level context (often referred to as sensitivity to stimulus statistics), but the degree to which the human brainstem exhibits such neural adaptation is unclear. In six electroencephalography experiments with over 125 participants, we demonstrate that the response latency of the human brainstem is sensitive to the history of acoustic stimulation over a few tens of milliseconds. We further show that human brainstem responses adapt to sound-level context in, at least, the last 44 ms, but that neural sensitivity to sound-level context decreases when the time window over which acoustic stimuli need to be integrated becomes wider. Our study thus provides evidence of adaptation to sound-level context in the human brainstem and of the timescale over which sound-level information affects neural responses to sound. The research delivers an important link to studies on neural adaptation in non-human animals.

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A Neural Signature of Regularity in Sound is Reduced in Older Adults

Sensitivity to repetitions in sound amplitude and frequency is crucial for sound perception. As with other aspects of sound processing, sensitivity to such patterns may change with age, and may help explain some age-related changes in hearing such as segregating speech from background sound. We recorded magnetoencephalography to characterize differences in the processing of sound patterns between younger and older adults. We presented tone sequences that either contained a pattern (made of a repeated set of tones) or did not contain a pattern. We show that auditory cortex in older, compared to younger, adults is hyperresponsive to sound onsets, but that sustained neural activity in auditory cortex, indexing the processing of a sound pattern, is reduced. Hence, the sensitivity of neural populations in auditory cortex fundamentally differs between younger and older individuals, overresponding to sound onsets, while underresponding to patterns in sounds. This may help to explain some age-related changes in hearing such as increased sensitivity to distracting sounds and difficulties tracking speech in the presence of other sound.

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Parametric cognitive load reveals hidden costs in the neural processing of perfectly intelligible degraded speech

Speech is often degraded by environmental noise or hearing impairment. People can compensate for degradation, but this requires cognitive effort. Previous research has identified frontotemporal networks involved in effortful perception, but materials in these works were also less intelligible, and so it is not clear whether activity reflected effort or intelligibility differences. We used functional magnetic resonance imaging to assess the degree to which spoken sentences were processed under distraction, and whether this depended on speech quality even when intelligibility of degraded speech was matched to that of clear speech (i.e., 100%). On each trial, participants either attended to a sentence, or to a concurrent multiple object tracking (MOT) task that imposed parametric cognitive load. Activity in bilateral anterior insula reflected task demands: during the MOT task, activity increased as cognitive load increased, and during speech listening, activity increased as speech became more degraded. In marked contrast, activity in bilateral anterior temporal cortex was speech-selective, and gated by attention when speech was degraded. In this region, performance of the MOT task with a trivial load blocked processing of degraded speech whereas processing of clear speech was unaffected. As load increased, responses to clear speech in these areas declined, consistent with reduced capacity to process it. This result dissociates cognitive control from speech processing: substantially less cognitive control is required to process clear speech than is required to understand even very mildly degraded, 100% intelligible, speech. Perceptual and control systems clearly interact dynamically during real-world speech comprehension. Significance StatementSpeech is often perfectly intelligible even when degraded, e.g., by background sound, phone transmission, or hearing loss. How does degradation alter cognitive demands? Here, we use fMRI to demonstrate a novel and critical role for cognitive control in the processing of mildly degraded but perfectly intelligible speech. We compare speech that is matched for intelligibility but differs in putative control demands, dissociating cognitive control from speech processing. We also impose a parametric cognitive load during perception, dissociating processes that depend on tasks from those that depend on available capacity. Our findings distinguish between frontal and temporal contributions to speech perception and reveal a hidden cost to processing mildly degraded speech, underscoring the importance of cognitive control for everyday speech comprehension.

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Sustained neural activity correlates with rapid perceptual learning of auditory patterns

Repeating structures forming regular patterns are common in sounds. Learning such patterns may enable accurate perceptual organization. In five experiments, we investigated the behavioral and neural signatures of rapid perceptual learning of regular sound patterns. We show that recurring (compared to novel) patterns are detected more quickly and increase sensitivity to pattern deviations and to the temporal order of pattern onset relative to a visual stimulus. Sustained neural activity reflected perceptual learning in two ways. Firstly, sustained activity increased earlier for recurring than novel patterns when participants attended to sounds, but not when they ignored them; this earlier increase mirrored the rapid perceptual learning we observed behaviorally. Secondly, the magnitude of sustained activity was generally lower for recurring than novel patterns, but only for trials later in the experiment, and independent of whether participants attended to or ignored sounds. The late manifestation of sustained activity reduction suggests that it is not directly related to rapid perceptual learning, but to a mechanism that does not require attention to sound. In sum, we demonstrate that the latency of sustained activity reflects rapid perceptual learning of auditory patterns, while the magnitude may reflect a result of learning, such as better prediction of learned auditory patterns.

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Speech-evoked brain activity is more robust to competing speech when it is spoken by someone familiar

People are much better at understanding speech when it is spoken by a familiar talker--such as a friend or partner--than when the interlocutor is unfamiliar. This provides an opportunity to examine the substrates of intelligibility and familiarity, independent of acoustics. Is the familiarity effect evident as early as primary auditory cortex, or only at later processing stages? Here, we presented sentences spoken by naturally familiar talkers (the participants friend or partner) and unfamiliar talkers (the friends or partners of other participants). We compared multivariate activity in speech-sensitive regions of cortex between conditions in which target sentences were presented alone and conditions in which the same target sentences were presented at the same time as a competing sentence. Using representational similarity analysis (RSA), we demonstrate that the pattern of activity evoked by a spoken sentence is less degraded by the presence of a competing sentence when it is spoken by a friend or partner than by someone unfamiliar; the results cannot be explained by acoustic differences since familiar and unfamiliar talkers were nearly identical across the group. This familiar-voice advantage is most prominent in nonprimary auditory cortical areas, along the posterior superior and middle temporal gyri. Across participants, the magnitude of the familiar-unfamiliar RSA difference correlates with the familiar-voice benefit to intelligibility. Overall, our results demonstrate that experience-driven improvements in intelligibility are associated with enhanced patterns of neural activity in nonprimary auditory cortical areas. Significance statementSpeech is a complex signal, and we do not yet fully understand how the content of a spoken sentence is encoded in cortex. Here, we used a novel approach based on analysing multivariate activity: we compared activity evoked by highly intelligible sentences presented alone and by the same sentences presented with a competing masker. The distributed pattern of activity in speech-sensitive regions of the brain was more similar between the alone and masker conditions when the target sentence was spoken by someone familiar--the participants friend or partner--than someone unfamiliar. This metric correlated with the intelligibility of the familiar voice. These results imply that the spatial pattern of activity in speech-sensitive regions reflects the intelligibility of a spoken sentence.

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A Novel Approach to Investigate Subcortical and Cortical Sensitivity to Temporal Structure Simultaneously

Hearing loss is associated with changes at the peripheral, subcortical, and cortical auditory stages. Research often focuses on these stages in isolation, but peripheral damage has cascading effects on central processing, and different stages are interconnected through extensive feedforward and feedback projections. Accordingly, assessment of the entire auditory system is needed to understand auditory pathology. Using a novel stimulus paired with electroencephalography in young, normal-hearing adults, we assess neural function at multiple stages of the auditory pathway simultaneously. We employ click trains that repeatedly accelerate then decelerate (3.5 Hz frequency modulation; FM) introducing varying inter-click-intervals (4 to 40 ms). We measured the amplitude of cortical potentials, and the latencies and amplitudes of Waves III and V of the auditory brainstem response (ABR), to clicks as a function of preceding inter-click-interval. This allowed us to assess cortical processing of frequency modulation, as well as adaptation and neural recovery time in subcortical structures (probably cochlear nuclei and inferior colliculi). Subcortical adaptation to inter-click intervals was reflected in longer latencies. Cortical responses to the 3.5 Hz FM included phase-locking, probably originating from auditory cortex, and sustained activity likely originating from higher-level cortices. We did not observe any correlations between subcortical and cortical responses. By recording neural responses from different stages of the auditory system simultaneously, we can study functional relationships among levels of the auditory system, which may provide a new and helpful window on hearing and hearing impairment.

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Pupil dilation is sensitive to semantic ambiguity and acoustic degradation

Speech comprehension is often challenged by background noise or other acoustic interference. It can also be challenged by linguistic factors, such as complex syntax, or the presence of words with more than one meaning. Pupillometry is increasingly recognized as a technique that provides a window onto acoustic challenges, but this work has not been well integrated with an older literature linking pupil dilation to "mental effort", which would include linguistic challenges. Here, we measured pupil dilation while listeners heard spoken sentences with clear sentence-level meaning that contained words with more than one meaning ("The shell was fired towards the tank") or matched sentences without ambiguous words ("Her secrets were written in her diary"). This semantic-ambiguity manipulation was crossed with an acoustic manipulation: two levels of a 30-talker babble masker in Experiment 1; and presence or absence of a pink noise masker in Experiment 2. Speech comprehension, indexed by a semantic relatedness task, was high (above 82% correct) in all conditions. Pupils dilated when sentences included semantically ambiguous words compared to matched sentences and when maskers were present compared to absent (Experiment 2) or were more compared to less intense (Experiment 1). The current results reinforce the idea that many different challenges to speech comprehension, that afford different cognitive processes and are met by the brain in different ways, manifest as an increase in pupil dilation.

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Neural responses and perceptual sensitivity to sound depend on sound-level statistics

Sensitivity to sound-level statistics is crucial for optimal perception, but research has focused mostly on neurophysiological recordings, whereas behavioral evidence is sparse. We use electroencephalography (EEG) and behavioral methods to investigate how sound-level statistics affect neural activity and the detection of near-threshold changes in sound amplitude. We presented noise bursts with sound levels drawn from distributions with either a low or a high modal sound level. One participant group listened to the stimulation while EEG was recorded (Experiment I). A second group performed a behavioral amplitude-modulation detection task (Experiment II). Neural activity depended on sound-level statistical context in two different ways. Consistent with an account positing that the sensitivity of neurons to sound intensity adapts to ambient sound level, responses for higher-intensity bursts were larger in low-mode than high-mode contexts, whereas responses for lower-intensity bursts did not differ between contexts. In contrast, a concurrent slow neural response indicated prediction-error processing: The response was larger for bursts at intensities that deviated from the predicted statistical context compared to those not deviating. Behavioral responses were consistent with prediction-error processing, but not with neural adaptation. Hence, neural activity adapts to sound-level statistics, but fine-tuning of perceptual sensitivity appears to involve neural prediction-error responses.

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Motor planning modulates neural activity patterns in early human auditory cortex

It is well established that movement planning recruits motor-related cortical brain areas in preparation for the forthcoming action. Given that an integral component to the control of action is the processing of sensory information throughout movement, we predicted that movement planning might also modulate early sensory cortical areas, readying them for sensory processing during the unfolding action. To test this hypothesis, we performed two human functional MRI studies involving separate delayed movement tasks and focused on pre-movement neural activity in early auditory cortex, given its direct connections to the motor system and evidence that it is modulated by motor cortex during movement in rodents. We show that effector-specific information (i.e., movements of the left vs. right hand in Experiment 1, and movements of the hand vs. eye in Experiment 2) can be decoded, well before movement, from neural activity in early auditory cortex. We find that this motor-related information is represented in a separate subregion of auditory cortex than sensory-related information and is present even when movements are cued visually instead of auditorily. These findings suggest that action planning, in addition to preparing the motor system for movement, involves selectively modulating primary sensory areas based on the intended action.

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A sound-sensitive source of alpha oscillations in human non-primary auditory cortex

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschls gyrus (HG) with pronounced induced high-frequency (70-150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however their distribution within auditory cortex has not been established. Alpha activity (7-14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (four female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function.\n\nSignificance StatementTo understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7-14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschls gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.

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The effects of aging on neural signatures of temporal regularity processing in sounds

Sensitivity to temporal regularity (e.g., amplitude modulation) is crucial for speech perception. Degradation of the auditory periphery due to aging and hearing loss may lead to an increased response gain in auditory cortex, with potential consequences for the processing of temporal regularities. We used electroencephalography recorded from younger (18-33 years) and older (55-80 years) adults to investigate how aging affects neural gain and the neural sensitivity to amplitude modulation in sounds. Aging was associated with reduced adaptation in auditory cortex, suggesting an age-related gain increase. Consistently, neural synchronization in auditory cortex to a 4-Hz amplitude modulation of a narrow-band noise was enhanced in ~30% of older individuals. Despite enhanced responsivity in auditory cortex, sustained neural activity (likely involving auditory and higher-order brain regions) in response to amplitude modulation was absent in older people. Hence, aging may lead to an over-responsivity to amplitude modulation in auditory cortex, but to a diminished regularity representation in higher-order areas.

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Neural signatures of the processing of temporal patterns in sounds

The ability to detect regularities in sound (i.e., recurring structure) is critical for effective perception, enabling, for example, change detection and prediction. Two seemingly unconnected lines of research concern the neural operations involved in processing regularities: one investigates how neural activity synchronizes with temporal regularities (e.g., frequency modulation; FM) in sounds, whereas the other focuses on increases in sustained activity during stimulation with repeating tone-frequency patterns. In three electroencephalography studies with male and female human participants, we investigated whether neural synchronization and sustained neural activity are dissociable, or whether they are functionally interdependent. Experiment I demonstrated that neural activity synchronizes with temporal regularity (FM) in sounds, and that sustained activity increases concomitantly. In Experiment II, phase coherence of FM in sounds was parametrically varied. Although neural synchronization was more sensitive to changes in FM coherence, such changes led to a systematic modulation of both neural synchronization and sustained activity, with magnitude increasing as coherence increased. In Experiment III, participants either performed a duration categorization task on the sounds, or a visual object tracking task to distract attention. Neural synchronization was observed irrespective of task, whereas the sustained response was observed only when attention was on the auditory task, not under (visual) distraction. The results suggest that neural synchronization and sustained activity levels are functionally linked: both are sensitive to regularities in sounds. However, neural synchronization might reflect a more sensory-driven response to regularity, compared with sustained activity which may be influenced by attentional, contextual, or other experiential factors.\n\nSignificance statementOptimal perception requires that the auditory system detects regularities in sounds. Synchronized neural activity and increases in sustained neural activity both appear to index the detection of a regularity, but the functional interrelation of these two neural signatures is unknown. In three electroencephalography experiments, we measured both signatures concomitantly while listeners were presented with sounds containing frequency modulations that differed in their regularity. We observed that both neural signatures are sensitive to temporal regularity in sounds, although they functionally decouple when a listener is distracted by a demanding visual task. Our data suggest that neural synchronization reflects a more automatic response to regularity, compared with sustained activity which may be influenced by attentional, contextual, or other experiential factors.

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