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.

Highlights

  • Aging is characterized by marked declines in sensory and cognitive functions [1,2,3,4], and a vast literature implicates such agerelated changes to co-occur with differences in functionally localized cortical activity [5,6,7,8], but in disrupted functional interactions spanning distributed, complex brain networks [9,10,11,12]

  • Cortical network construction We constructed weighted functional networks for each subject by assigning connections based on the inter-regional correlation of functional magnetic resonance imaging (fMRI) responses between 66 cortical regions specified in the Desikan-Killiany atlas, after projecting subjects’ functional data onto cortical surface maps using Freesurfer and SUMA software [49,50,51]

  • Contrary to previous reports [26], our results suggest that age-related differences in functional network organization are not task-independent, as the group differences were modulated by the listening condition

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Summary

Introduction

Aging is characterized by marked declines in sensory and cognitive functions [1,2,3,4], and a vast literature implicates such agerelated changes to co-occur with differences in functionally localized cortical activity [5,6,7,8], but in disrupted functional interactions spanning distributed, complex brain networks [9,10,11,12]. Previous studies have established that brain structural and functional networks maintain a small-world organization optimized for both high local and global efficiency of information transfer [17,18,19] This small-world organization balances opposing demands for segregated (localized) and integrated (distributed) processing, both hypothesized to be crucial for higher-level cognition [20,21,22]. Recent findings by Achard & Bullmore (2007) and Wang et al (2010) indicate reduced efficiency of global information transfer in older adult networks during both rest and memory task performance [26,29], suggesting that age-related cognitive deficits could be associated with declines in efficient small-world organization

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