Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity.

Abstract

The reliable neuroimaging finding that older adults often show greater activity (over-recruitment) than younger adults is typically attributed to compensation. Yet, the neural mechanisms of over-recruitment in older adults (OAs) are largely unknown. Rodent electrophysiology studies have shown that as number of afferent fibers within a circuit decreases with age, the fibers that remain show higher synaptic field potentials (less wiring, more firing). Extrapolating to system-level measures in humans, we proposed and tested the hypothesis that greater activity in OAs compensates for impaired white-matter connectivity. Using a neuropsychological test battery, we measured individual differences in executive functions associated with the prefrontal cortex (PFC) and memory functions associated with the medial temporal lobes (MTLs). Using event-related functional magnetic resonance imaging, we compared activity for successful versus unsuccessful trials during a source memory task. Finally, we measured white-matter integrity using diffusion tensor imaging. The study yielded 3 main findings. First, low-executive OAs showed greater success-related activity in the PFC, whereas low-memory OAs showed greater success-related activity in the MTLs. Second, low-executive OAs displayed white-matter deficits in the PFC, whereas low-memory OAs displayed white-matter deficits in the MTLs. Finally, in both prefrontal and MTL regions, white-matter decline and success-related activations occurred in close proximity and were negatively correlated. This finding supports the less-wiring-more-firing hypothesis, which provides a testable account of compensatory over-recruitment in OAs.

Department

Description

Provenance

Citation

Published Version (Please cite this version)

10.1093/cercor/bht289

Publication Info

Daselaar, Sander M, Vijeth Iyengar, Simon W Davis, Karl Eklund, Scott M Hayes and Roberto E Cabeza (2015). Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity. Cereb Cortex, 25(4). pp. 983–990. 10.1093/cercor/bht289 Retrieved from https://hdl.handle.net/10161/10281.

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Scholars@Duke

Davis

Simon Wilton Davis

Associate Professor in Neurology

My research centers around the use of structural and functional imaging measures to study the shifts in network architecture in the aging brain. I am specifically interested in changes in how changes in structural and functional connectivity associated with aging impact the semantic retrieval of word or fact knowledge. Currently this involves asking why older adults have particular difficulty in certain kinds of semantic retrieval, despite the fact that vocabularies and knowledge stores typically improve with age.

A second line of research involves asking questions about how this semantic system is organized in young adults, understanding which helps form a basis for asking questions about older adults. To what degree are these semantic retrieval processes lateralized? What cognitive factors affect this laterality? How are brain structures like the corpus callosum involved in mediating distributed activation patterns associated with semantic retrieval? 

Cabeza

Roberto Cabeza

Professor of Psychology and Neuroscience

My laboratory investigates the neural correlates of memory and cognition in young and older adults using fMRI. We have three main lines of research: First, we distinguish the neural correlates of various episodic memory processes. For example, we have compared encoding vs. retrieval, item vs. source memory, recall vs. recognition, true vs. false memory, and emotional vs. nonemotional memory. We are particularly interested in the contribution of prefrontal cortex (PFC) and medial temporal lobe (MTL) subregions and their interactions. Second, we investigate similarities and differences between the neural correlates of episodic memory and other memory and cognitive functions (working, semantic, implicit, and procedural memory; attention; perception, etc.). The main goal of this cross-functional approach is to understand the contributions of brain regions shared by different cognitive functions. Finally, in both episodic memory and cross-function studies, we also examine the effects of healthy and pathological aging. Regarding episodic memory, we have linked processes differentially affected by aging (e.g., item vs. source memory, recall vs. recognition) to the effects of aging on specific PFC and MTL subregions. Regarding cross-function comparisons, we identify age-related changes in activity that are common to various functions. For example, we have found an age-related increase in bilaterality that occurs for many functions (memory, attention, language, perception, and motor) and is associated with functional compensation.


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