The impact of parkinson's disease on the cortical mechanisms that support auditory–motor integration for voice control

Huang, Xiyan; Chen, Xi; Yan, Nan; Jones, Jeffery A.; Wang, Emily; Chen, Ling; Guo, Zhiqiang; Liu, Weifeng; Liu, Peng; Liu, Hanjun

doi:10.1002/hbm.23306

Cited by 68 publications

(108 citation statements)

References 74 publications

(191 reference statements)

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“…Abnormal vocal behavior towards altered auditory feedback was also reported in patients with Parkinson's disease in several previous experiments (Chen, et al, 2013,Huang, et al, 2016,Liu, et al, 2012,Mollaei, et al, 2013). Like the AD patients in the current study Patients with Parkinson's disease also showed an elevated pitch-compensatory response (Chen, et al, 2013,Huang, et al, 2016).…”

Section: Discussionsupporting

confidence: 67%

“…Like the AD patients in the current study Patients with Parkinson's disease also showed an elevated pitch-compensatory response (Chen, et al, 2013,Huang, et al, 2016). Further, the Parkinson's disease patients also showed an elevated amplitude-compensatory response in experiments where amplitude was perturbed in the feedback signal (Liu, et al, 2012).…”

Section: Discussionsupporting

confidence: 56%

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Abnormal vocal behavior predicts executive and memory deficits in Alzheimer's disease

Ranasinghe

Gill

Kothare

et al. 2017

Neurobiology of Aging

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Speakers respond automatically and rapidly to compensate for brief perturbations of pitch in their auditory feedback. The specific adjustments in vocal output require integration of brain regions involved in speech-motor-control in order to detect the sensory-feedback-error and implement the motor-correction. Cortical regions involved in the pitch-reflex phenomenon are highly vulnerable targets of network disruption in Alzheimer's disease (AD). We examined the pitch-reflex in AD patients (n=19) compared to an age-matched control group (n=16). We measured the degree of behavioral compensation (peak-compensation) and the extent of the adaptive response (pitch-response-persistence). Healthy-controls reached a peak-compensation of 18.7±0.8 cents, and demonstrated a sustained compensation at 8.9±0.69 cents. AD patients, in contrast, demonstrated a significantly elevated peak-compensation (22.4±1.2 cents, P<0.05), and a reduced sustained response (pitch-response-persistence, 4.5±0.88 cents, P<0.001). The degree of increased peak-compensation predicted executive dysfunction, while the degree of impaired pitch-response-persistence predicted memory dysfunction, in AD patients. The current study demonstrates pitch-reflex as a sensitive behavioral index of impaired prefrontal modulation of sensorimotor integration, and compromised plasticity mechanisms of memory, in AD.

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Section: Discussionsupporting

confidence: 67%

Section: Discussionsupporting

confidence: 56%

Abnormal vocal behavior predicts executive and memory deficits in Alzheimer's disease

Ranasinghe

Gill

Kothare

et al. 2017

Neurobiology of Aging

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“…The STG cluster identified in the present study corresponds closely to an anterolateral region of Heschl's gyrus that electrocorticography data has linked to online voice error correction following rapid perturbations in auditory feedback (Behroozmand et al., 2016). Compared to healthy individuals, those with PD respond to rapid perturbations in auditory feedback with an exaggerated compensation in vocal output compared to healthy controls (Chen et al., 2013; Huang et al., 2016; Liu, Wang, Metman, & Larson, 2012). It has thus been suggested that people with PD have impaired feedforward control of speech production and, as a result, rely more heavily on sensory feedback integration (Liu et al., 2012).…”

Section: Discussionmentioning

confidence: 99%

“…Our findings raise the possibility that, in addition to impaired feedforward control, there may be impaired auditory feedback integration mediated by decreased connectivity between left putamen and left STG. For example, not only do people with PD respond to rapid auditory perturbations with exaggerated vocal responses (Chen et al., 2013; Huang et al., 2016; Liu et al., 2012), they also appear to compensate less than controls when adapting to long‐term alterations in auditory feedback (Mollaei, Shiller, & Gracco, 2013). Decreased coupling of left putamen and left STG could thus reflect difficulties in integrating sensory information during speech production in PD.…”

Section: Discussionmentioning

confidence: 99%

Altered resting‐state functional connectivity of the putamen and internal globus pallidus is related to speech impairment in Parkinson's disease

et al. 2018

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IntroductionSpeech impairment in Parkinson's disease (PD) is pervasive, with life‐impacting consequences. Yet, little is known about how functional connections between the basal ganglia and cortex relate to PD speech impairment (PDSI). Whole‐brain resting‐state connectivity analyses of basal ganglia nuclei can expand the understanding of PDSI pathophysiology.MethodsResting‐state data from 89 right‐handed subjects were downloaded from the Parkinson's Progression Markers Initiative database. Subjects included 12 older healthy controls (“OHC”), 42 PD patients without speech impairment (“PDN”), and 35 PD subjects with speech impairment (“PDSI”). Subjects were assigned to PDN and PDSI groups based on the Movement Disorders Society Unified Parkinson's Disease Rating Scale (MDS‐UPDRS) Part III speech item scores (“0” vs. “1–4”). Whole‐brain functional connectivity was calculated for four basal ganglia seeds in each hemisphere: putamen, caudate, external globus pallidus (GPe), and internal globus pallidus (GPi). For each seed region, group‐averaged connectivity maps were compared among OHC, PDN, and PDSI groups using a multivariate ANCOVA controlling for the effects of age and sex. Subsequent planned pairwise t‐tests were performed to determine differences between the three groups using a voxel‐wise threshold of p < 0.001 and cluster‐extent threshold of 272 mm3 (FWE<0.05).ResultsIn comparison with OHCs, both PDN and PDSI groups demonstrated significant differences in cortical connectivity with bilateral putamen, bilateral GPe, and right caudate. Compared to the PDN group, the PDSI subjects demonstrated significant differences in cortical connectivity with left putamen and left GPi. PDSI subjects had lower connectivity between the left putamen and left superior temporal gyrus compared to PDN. In addition, PDSI subjects had greater connectivity between left GPi and three cortical regions: left dorsal premotor/laryngeal motor cortex, left angular gyrus, and right angular gyrus.ConclusionsThe present findings suggest that speech impairment in PD is associated with altered cortical connectivity with left putamen and left GPi.

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“…Accumulating evidence has shown that P2 component reflects not only the central auditory processing (e.g., error detection) but also the feedback-based motor processing (e.g., error correction) in the online monitoring of vocal production. For example, when compensating for pitch perturbations in voice auditory feedback, individuals with Parkinson's disease produced significantly larger P2 responses than healthy controls due to enhanced activity in the brain regions including the STG, PMC, and IFG (Huang et al, 2016). Also, P2 responses were found to be significantly correlated with regional homogeneity of those brain regions in the resting-state (Guo et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Menstrual Cycle Phase Modulates Auditory-Motor Integration for Vocal Pitch Regulation

Liu

Niu²,

Liu

et al. 2016

Front. Neurosci.

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In adult females, previous work has demonstrated that changes in auditory function and vocal motor behaviors may accompany changes in gonadal steroids. Less is known, however, about the influence of gonadal steroids on auditory-motor integration for voice control in humans. The present event-related potential (ERP) study sought to examine the interaction between gonadal steroids and auditory feedback-based vocal pitch regulation across the menstrual cycle. Participants produced sustained vowels while hearing their voice unexpectedly pitch-shifted during the menstrual, follicular, and luteal phases of the menstrual cycle. Measurement of vocal and cortical responses to pitch feedback perturbations and assessment of estradiol and progesterone levels were performed in all three phases. The behavioral results showed that the menstrual phase (when estradiol levels are low) as associated with larger magnitudes of vocal responses than the follicular and luteal phases (when estradiol levels are high). Furthermore, there was a significant negative correlation between the magnitudes of vocal responses and estradiol levels. At the cortical level, ERP P2 responses were smaller during the luteal phase (when progesterone levels were high) than the menstrual and follicular phases (when progesterone levels were low). These findings show neurobehavioral evidence for the modulation of auditory-motor integration for vocal pitch regulation across the menstrual cycle, and provide important insights into the neural mechanisms and functional outcomes of gonadal steroids' influence on speech motor control in adult women.

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The impact of parkinson's disease on the cortical mechanisms that support auditory–motor integration for voice control

Cited by 68 publications

References 74 publications

Abnormal vocal behavior predicts executive and memory deficits in Alzheimer's disease

Abnormal vocal behavior predicts executive and memory deficits in Alzheimer's disease

Altered resting‐state functional connectivity of the putamen and internal globus pallidus is related to speech impairment in Parkinson's disease

Menstrual Cycle Phase Modulates Auditory-Motor Integration for Vocal Pitch Regulation

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