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Large-scale cortical functional organization and speech perception across the lifespan.

ABSTRACT: Aging is accompanied by substantial changes in brain function, including functional reorganization of large-scale brain networks. Such differences in network architecture have been reported both at rest and during cognitive task performance, but an open question is whether these age-related differences show task-dependent effects or represent only task-independent changes attributable to a common factor (i.e., underlying physiological decline). To address this question, we used graph theoretic analysis to construct weighted cortical functional networks from hemodynamic (functional MRI) responses in 12 younger and 12 older adults during a speech perception task performed in both quiet and noisy listening conditions. Functional networks were constructed for each subject and listening condition based on inter-regional correlations of the fMRI signal among 66 cortical regions, and network measures of global and local efficiency were computed. Across listening conditions, older adult networks showed significantly decreased global (but not local) efficiency relative to younger adults after normalizing measures to surrogate random networks. Although listening condition produced no main effects on whole-cortex network organization, a significant age group x listening condition interaction was observed. Additionally, an exploratory analysis of regional effects uncovered age-related declines in both global and local efficiency concentrated exclusively in auditory areas (bilateral superior and middle temporal cortex), further suggestive of specificity to the speech perception tasks. Global efficiency also correlated positively with mean cortical thickness across all subjects, establishing gross cortical atrophy as a task-independent contributor to age-related differences in functional organization. Together, our findings provide evidence of age-related disruptions in cortical functional network organization during speech perception tasks, and suggest that although task-independent effects such as cortical atrophy clearly underlie age-related changes in cortical functional organization, age-related differences also demonstrate sensitivity to task domains.

SUBMITTER: Sheppard JP

PROVIDER: S-EPMC3031590 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Large-scale cortical functional organization and speech perception across the lifespan.

Sheppard John P JP Wang Ji-Ping JP Wong Patrick C M PC

PloS one 20110131 1

Aging is accompanied by substantial changes in brain function, including functional reorganization of large-scale brain networks. Such differences in network architecture have been reported both at rest and during cognitive task performance, but an open question is whether these age-related differences show task-dependent effects or represent only task-independent changes attributable to a common factor (i.e., underlying physiological decline). To address this question, we used graph theoretic a ...[more]

PMID: 21304991

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Project description:Impaired speech perception in noise despite normal peripheral auditory function is a common problem in young adults. Despite a growing body of research, the pathophysiology of this impairment remains unknown. This magnetoencephalography study characterizes the cortical tracking of speech in a multi-talker background in a group of highly selected adult subjects with impaired speech perception in noise without peripheral auditory dysfunction. Magnetoencephalographic signals were recorded from 13 subjects with impaired speech perception in noise (six females, mean age: 30 years) and matched healthy subjects while they were listening to 5 different recordings of stories merged with a multi-talker background at different signal to noise ratios (No Noise, +10, +5, 0 and -5 dB). The cortical tracking of speech was quantified with coherence between magnetoencephalographic signals and the temporal envelope of (i) the global auditory scene (i.e. the attended speech stream and the multi-talker background noise), (ii) the attended speech stream only and (iii) the multi-talker background noise. Functional connectivity was then estimated between brain areas showing altered cortical tracking of speech in noise in subjects with impaired speech perception in noise and the rest of the brain. All participants demonstrated a selective cortical representation of the attended speech stream in noisy conditions, but subjects with impaired speech perception in noise displayed reduced cortical tracking of speech at the syllable rate (i.e. 4-8 Hz) in all noisy conditions. Increased functional connectivity was observed in subjects with impaired speech perception in noise in Noiseless and speech in noise conditions between supratemporal auditory cortices and left-dominant brain areas involved in semantic and attention processes. The difficulty to understand speech in a multi-talker background in subjects with impaired speech perception in noise appears to be related to an inaccurate auditory cortex tracking of speech at the syllable rate. The increased functional connectivity between supratemporal auditory cortices and language/attention-related neocortical areas probably aims at supporting speech perception and subsequent recognition in adverse auditory scenes. Overall, this study argues for a central origin of impaired speech perception in noise in the absence of any peripheral auditory dysfunction.

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Large-scale cortical functional organization and speech perception across the lifespan.

Publications

Large-scale cortical functional organization and speech perception across the lifespan.

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