Age-related top-down suppression deficit in the early stages of cortical visual memory processing

Gazzaley, Adam; Clapp, Wesley; Kelley, Jon; McEvoy, Kevin; Knight, Robert T.; D'Esposito, Mark · 2008 · OpenAlex-citations

DOI: 10.1073/pnas.0806074105

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Summary

This study investigates the neural mechanisms underlying age-related cognitive decline by examining the relationship between two leading theories: the inhibitory deficit hypothesis and the processing speed hypothesis. While previous functional magnetic resonance imaging (fMRI) research indicated that older adults struggle to suppress task-irrelevant information during visual working memory (WM) encoding, fMRI’s low temporal resolution prevented precise timing analysis. To address this, the authors used electroencephalography (EEG) to determine whether age-related suppression deficits are abolished or merely delayed, and how this interacts with general processing speed declines. The researchers recorded 64-channel EEG data from 19 younger adults (19–33 years) and 22 older adults (60–72 years) performing a selective WM task. Participants viewed sequences of faces and natural scenes under three conditions: remembering faces while ignoring scenes, remembering scenes while ignoring faces, or passively viewing stimuli. This design allowed for the dissociation of neural responses to relevant, irrelevant, and passive stimuli. The analysis focused on posterior EEG components (P1, N1, gamma synchronization, P300, and alpha desynchronization) and frontal midline theta power to assess top-down modulation across the visual processing timeline. Behavioral results showed that older adults had significantly lower recognition accuracy for both faces and scenes, though response times did not differ significantly between groups. Neural analysis revealed that younger adults exhibited robust top-down enhancement for relevant stimuli and suppression for irrelevant stimuli across all measured time windows. In contrast, older adults showed preserved enhancement but a selective deficit in suppressing irrelevant information during early processing stages (P1 amplitude at 50–150 ms and N1 latency at 120–220 ms). Crucially, older adults demonstrated intact suppression in later stages (alpha desynchronization at 500–650 ms), indicating that inhibitory mechanisms are not lost but delayed. Furthermore, frontal midline theta analysis showed that older adults invested greater overall effort but failed to differentiate neural activity between relevant and irrelevant stimuli early in the trial. Subgroup analysis confirmed that older adults with poorer WM performance exhibited the most significant early suppression deficits. These findings reconcile the inhibitory deficit and processing speed hypotheses by demonstrating that age-related cognitive impairment stems from a dynamic interaction between both factors. Older adults experience a generalized slowing of neural processing, which specifically delays the deployment of top-down suppression. This delay allows irrelevant information to interfere with working memory before compensatory mechanisms can engage. The study provides electrophysiological evidence that the inability to filter distractions early in the visual processing stream is a primary driver of WM decline in normal aging, rather than a complete loss of inhibitory control.

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• cognitive aging