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Altered functional connectivity during speech perception in congenital amusia.

ABSTRACT: Individuals with congenital amusia have a lifelong history of unreliable pitch processing. Accordingly, they downweight pitch cues during speech perception and instead rely on other dimensions such as duration. We investigated the neural basis for this strategy. During fMRI, individuals with amusia (N = 15) and controls (N = 15) read sentences where a comma indicated a grammatical phrase boundary. They then heard two sentences spoken that differed only in pitch and/or duration cues and selected the best match for the written sentence. Prominent reductions in functional connectivity were detected in the amusia group between left prefrontal language-related regions and right hemisphere pitch-related regions, which reflected the between-group differences in cue weights in the same groups of listeners. Connectivity differences between these regions were not present during a control task. Our results indicate that the reliability of perceptual dimensions is linked with functional connectivity between frontal and perceptual regions and suggest a compensatory mechanism.

SUBMITTER: Jasmin K

PROVIDER: S-EPMC7449693 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Altered functional connectivity during speech perception in congenital amusia.

Jasmin Kyle K Dick Frederic F Stewart Lauren L Tierney Adam Taylor AT

eLife 20200807

Individuals with congenital amusia have a lifelong history of unreliable pitch processing. Accordingly, they downweight pitch cues during speech perception and instead rely on other dimensions such as duration. We investigated the neural basis for this strategy. During fMRI, individuals with amusia (N = 15) and controls (N = 15) read sentences where a comma indicated a grammatical phrase boundary. They then heard two sentences spoken that differed only in pitch and/or duration cues and selected ...[more]

PMID: 32762842

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Project description:Aging affects pain experience and brain functioning. However, how aging leads to changes in pain perception and brain functional connectivity has not yet been completely understood. To investigate resting-state and pain perception changes in old and young participants, this study employed region of interest (ROI) to ROI resting-state functional connectivity (rsFC) analysis of imaging data by using regions implicated in sensory and affective dimensions of pain, descending pain modulation, and the default-mode networks (DMNs). Thirty-seven older (66.86 ± 4.04 years; 16 males) and 38 younger healthy participants (20.74 ± 4.15 years; 19 males) underwent 10 min' eyes-closed resting-state scanning. We examined the relationship between rsFC parameters with pressure pain thresholds. Older participants showed higher pain thresholds than younger. Regarding rsFC, older adults displayed increased connectivity of pain-related sensory brain regions in comparison to younger participants: increased rsFC between bilateral primary somatosensory area (SI) and anterior cingulate cortex (ACC), and between SI(L) and secondary somatosensory area (SII)-(R) and dorsolateral prefrontal cortex (PFC). Moreover, decreased connectivity in the older compared to the younger group was found among descending pain modulatory regions: between the amygdala(R) and bilateral insula(R), thalamus(R), ACC, and amygdala(L); between the amygdala(L) and insula(R) and bilateral thalamus; between ACC and bilateral insula, and between periaqueductal gray (PAG) and bilateral thalamus. Regarding the DMN, the posterior parietal cortex and lateral parietal (LP; R) were more strongly connected in the older group than in the younger group. Correlational analyses also showed that SI(L)-SII(R) rsFC was positively associated with pressure pain thresholds in older participants. In conclusion, these findings suggest a compensatory mechanism for the sensory changes that typically accompanies aging. Furthermore, older participants showed reduced functional connectivity between key nodes of the descending pain inhibitory pathway.

Project description:In everyday conversation, we usually process the talker's face as well as the sound of the talker's voice. Access to visual speech information is particularly useful when the auditory signal is degraded. Here, we used fMRI to monitor brain activity while adult humans (n = 60) were presented with visual-only, auditory-only, and audiovisual words. The audiovisual words were presented in quiet and in several signal-to-noise ratios. As expected, audiovisual speech perception recruited both auditory and visual cortex, with some evidence for increased recruitment of premotor cortex in some conditions (including in substantial background noise). We then investigated neural connectivity using psychophysiological interaction analysis with seed regions in both primary auditory cortex and primary visual cortex. Connectivity between auditory and visual cortices was stronger in audiovisual conditions than in unimodal conditions, including a wide network of regions in posterior temporal cortex and prefrontal cortex. In addition to whole-brain analyses, we also conducted a region-of-interest analysis on the left posterior superior temporal sulcus (pSTS), implicated in many previous studies of audiovisual speech perception. We found evidence for both activity and effective connectivity in pSTS for visual-only and audiovisual speech, although these were not significant in whole-brain analyses. Together, our results suggest a prominent role for cross-region synchronization in understanding both visual-only and audiovisual speech that complements activity in integrative brain regions like pSTS.SIGNIFICANCE STATEMENT In everyday conversation, we usually process the talker's face as well as the sound of the talker's voice. Access to visual speech information is particularly useful when the auditory signal is hard to understand (e.g., background noise). Prior work has suggested that specialized regions of the brain may play a critical role in integrating information from visual and auditory speech. Here, we show a complementary mechanism relying on synchronized brain activity among sensory and motor regions may also play a critical role. These findings encourage reconceptualizing audiovisual integration in the context of coordinated network activity.

Dataset Information

Altered functional connectivity during speech perception in congenital amusia.

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Altered functional connectivity during speech perception in congenital amusia.

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