Compensation or inhibitory failure? Testing hypotheses of age-related right frontal lobe involvement in verbal memory ability using structural and diffusion MRI

Simon R Cox,Mark E Bastin,Karen J Ferguson,Mike Allerhand,Natalie A Royle,Susanna Muñoz Maniega,John M Starr,Alasdair M.J Maclullich,Joanna M Wardlaw,Ian J Deary,Sarah E Macpherson

doi:10.1016/j.cortex.2014.08.001

Simon R Cox, Mark E Bastin + Show 9 more

Open Access

https://doi.org/10.1016/j.cortex.2014.08.001

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Journal: Cortex	Publication Date: Aug 21, 2014
Citations: 19	License type: cc-by

Affiliation: University of Edinburgh, Alzheimer Scotland

Abstract

Functional neuroimaging studies report increased right prefrontal cortex (PFC) involvement during verbal memory tasks amongst low-scoring older individuals, compared to younger controls and their higher-scoring contemporaries. Some propose that this reflects inefficient use of neural resources through failure of the left PFC to inhibit non-task-related right PFC activity, via the anterior corpus callosum (CC). For others, it indicates partial compensation – that is, the right PFC cannot completely supplement the failing neural network, but contributes positively to performance. We propose that combining structural and diffusion brain MRI can be used to test predictions from these theories which have arisen from fMRI studies. We test these hypotheses in immediate and delayed verbal memory ability amongst 90 healthy older adults of mean age 73 years. Right hippocampus and left dorsolateral prefrontal cortex (DLPFC) volumes, and fractional anisotropy (FA) in the splenium made unique contributions to verbal memory ability in the whole group. There was no significant effect of anterior callosal white matter integrity on performance. Rather, segmented linear regression indicated that right DLPFC volume was a significantly stronger positive predictor of verbal memory for lower-scorers than higher-scorers, supporting a compensatory explanation for the differential involvement of the right frontal lobe in verbal memory tasks in older age.

Highlights

IntroductionFunctional imaging studies of verbal memory tasks that compare activation patterns between young and older people show that older age is accompanied by “overrecruitment”; that is, greater cortical activation both in the brain regions engaged by young subjects, and in a more distributed network that has additional regions (reviewed in Craik & Rose, 2012; Goh, 2011; Park & Reuter-Lorenz, 2009)
Some aspects of memory functioning decline with age (Craik & Rose, 2012)
Functional imaging studies of verbal memory tasks that compare activation patterns between young and older people show that older age is accompanied by “overrecruitment”; that is, greater cortical activation both in the brain regions engaged by young subjects, and in a more distributed network that has additional regions

Summary

Introduction

Functional imaging studies of verbal memory tasks that compare activation patterns between young and older people show that older age is accompanied by “overrecruitment”; that is, greater cortical activation both in the brain regions engaged by young subjects, and in a more distributed network that has additional regions (reviewed in Craik & Rose, 2012; Goh, 2011; Park & Reuter-Lorenz, 2009). What this over-recruitment might represent is a matter of debate. We propose that the use of structural MRI data can provide an alternative perspective for testing hypotheses on this phenomenon that have arisen from the functional neuroimaging literature

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