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Neural correlates of abnormal auditory feedback processing during speech production in Alzheimer's disease.

ABSTRACT: Accurate integration of sensory inputs and motor commands is essential to achieve successful behavioral goals. A robust model of sensorimotor integration is the pitch perturbation response, in which speakers respond rapidly to shifts of the pitch in their auditory feedback. In a previous study, we demonstrated abnormal sensorimotor integration in patients with Alzheimer's disease (AD) with an abnormally enhanced behavioral response to pitch perturbation. Here we examine the neural correlates of the abnormal pitch perturbation response in AD patients, using magnetoencephalographic imaging. The participants phonated the vowel /α/ while a real-time signal processor briefly perturbed the pitch (100 cents, 400 ms) of their auditory feedback. We examined the high-gamma band (65-150 Hz) responses during this task. AD patients showed significantly reduced left prefrontal activity during the early phase of perturbation and increased right middle temporal activity during the later phase of perturbation, compared to controls. Activity in these brain regions significantly correlated with the behavioral response. These results demonstrate that impaired prefrontal modulation of speech-motor-control network and additional recruitment of right temporal regions are significant mediators of aberrant sensorimotor integration in patients with AD. The abnormal neural integration mechanisms signify the contribution of cortical network dysfunction to cognitive and behavioral deficits in AD.

SUBMITTER: Ranasinghe KG

PROVIDER: S-EPMC6450891 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Neural correlates of abnormal auditory feedback processing during speech production in Alzheimer's disease.

Ranasinghe Kamalini G KG Kothare Hardik H Kort Naomi N Hinkley Leighton B LB Beagle Alexander J AJ Mizuiri Danielle D Honma Susanne M SM Lee Richard R Miller Bruce L BL Gorno-Tempini Maria Luisa ML Vossel Keith A KA Houde John F JF Nagarajan Srikantan S SS

Scientific reports 20190405 1

Accurate integration of sensory inputs and motor commands is essential to achieve successful behavioral goals. A robust model of sensorimotor integration is the pitch perturbation response, in which speakers respond rapidly to shifts of the pitch in their auditory feedback. In a previous study, we demonstrated abnormal sensorimotor integration in patients with Alzheimer's disease (AD) with an abnormally enhanced behavioral response to pitch perturbation. Here we examine the neural correlates of ...[more]

PMID: 30952883

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

Project description:When we perform an action, its sensory outcomes usually follow shortly after. This characteristic temporal relationship aids in distinguishing self- from externally generated sensory input. To preserve this ability under dynamically changing environmental conditions, our expectation of the timing between action and outcome must be able to recalibrate, for example, when the outcome is consistently delayed. Until now, it remains unclear whether this process, known as sensorimotor temporal recalibration, can be specifically attributed to recalibration of sensorimotor (action-outcome) predictions, or whether it may be partly due to the recalibration of expectations about the intersensory (e.g., audio-tactile) timing. Therefore, we investigated the behavioral and neural correlates of temporal recalibration and differences in sensorimotor and intersensory contexts. During fMRI, subjects were exposed to delayed or undelayed tones elicited by actively or passively generated button presses. While recalibration of the expected intersensory timing (i.e., between the tactile sensation during the button movement and the tones) can be expected to occur during both active and passive movements, recalibration of sensorimotor predictions should be limited to active movement conditions. Effects of this procedure on auditory temporal perception and the modality-transfer to visual perception were tested in a delay detection task. Across both contexts, we found recalibration to be associated with activations in hippocampus and cerebellum. Context-dependent differences emerged in terms of stronger behavioral recalibration effects in sensorimotor conditions and were captured by differential activation pattern in frontal cortices, cerebellum, and sensory processing regions. These findings highlight the role of the hippocampus in encoding and retrieving newly acquired temporal stimulus associations during temporal recalibration. Furthermore, recalibration-related activations in the cerebellum may reflect the retention of multiple representations of temporal stimulus associations across both contexts. Finally, we showed that sensorimotor predictions modulate recalibration-related processes in frontal, cerebellar, and sensory regions, which potentially account for the perceptual advantage of sensorimotor versus intersensory temporal recalibration.

Dataset Information

Neural correlates of abnormal auditory feedback processing during speech production in Alzheimer's disease.

Publications

Neural correlates of abnormal auditory feedback processing during speech production in Alzheimer's disease.

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