Distinct aspects of frontal lobe structure mediate age-related differences in fluid intelligence and multitasking

Rogier A Kievit,Jodie Allen,Thea Kavanagh-Williamson,Teresa Cheung,Lauren Bates,Hayley Fisher,Simon W Davis,Dan Barnes,Diane Rowland,Anne Barcroft,John Sargeant,Tracy Thompson,Claire Hanley,David Troy,Melissa Fair,Beth Parkin,Andrew Hilton,Jason R Taylor,Liana Amunts,Cheryl Dias,Rhodri Cusack,Aldabra Stoddart,Marie Dixon,Sofia Gerbase,Beth Stevens,Tim Dalgleish,Kim Norman,Joanne Mitchell,Maggie Squire,Fiona Matthews,Cheryl Stone,Carol Brayne,Adarsh Grewal,Ozlem Yazlik,Andrew Gadie,Jaya Hillman,Gillian Amery,Lorraine K Tyler,Laura Villis,Jessica Penrose,Tina Emery,Anna Goulding,Linda Geerligs,Fiona Roby,Geoff Hale,Jonathan Dowrick,Patricia Johnston,Amanda Castle,Stanimira Georgieva,Nitin Williams,D N Mitchell ,Frances L Johnson ,Andrew C Calder ,Karen L Campbell ,Sharon Erzinçlioğlu ,William D Marslen–Wilson ,Edward T Bullmore ,James B Rowe ,Kamen A Tsvetanov ,Meredith A Shafto ,Alison M Mcminn ,Anna C Mccarrey ,John S Duncan ,Magdalena Kwaśniewska ,Richard N Henson

doi:10.1038/ncomms6658

Abstract

Ageing is characterized by declines on a variety of cognitive measures. These declines are often attributed to a general, unitary underlying cause, such as a reduction in executive function owing to atrophy of the prefrontal cortex. However, age-related changes are likely multifactorial, and the relationship between neural changes and cognitive measures is not well-understood. Here we address this in a large (N=567), population-based sample drawn from the Cambridge Centre for Ageing and Neuroscience (Cam-CAN) data. We relate fluid intelligence and multitasking to multiple brain measures, including grey matter in various prefrontal regions and white matter integrity connecting those regions. We show that multitasking and fluid intelligence are separable cognitive abilities, with differential sensitivities to age, which are mediated by distinct neural subsystems that show different prediction in older versus younger individuals. These results suggest that prefrontal ageing is a manifold process demanding multifaceted models of neurocognitive ageing.

Highlights

Ageing is characterized by declines on a variety of cognitive measures
Concurrent decline in grey matter (GM)[1] and white matter integrity (WMI)[6] of the frontal lobe has been observed in longitudinal samples, leading to an influential theory of ageing known as the frontal lobe hypothesis[7,8], in which declines in executive functions are attributed to age-related changes in the frontal lobe
We focus on four neural properties selected based on the current literature—(see Methods), two involving grey matter volume (GMV; Brodmann Area 10 (BA10) and the Multiple Demand (MD) System), and two involving WMI (the Forceps Minor (FM) and the Anterior Thalamic Radiations (ATR))

Summary

Introduction

Ageing is characterized by declines on a variety of cognitive measures. These declines are often attributed to a general, unitary underlying cause, such as a reduction in executive function owing to atrophy of the prefrontal cortex. We show that multitasking and fluid intelligence are separable cognitive abilities, with differential sensitivities to age, which are mediated by distinct neural subsystems that show different prediction in older versus younger individuals. These results suggest that prefrontal ageing is a manifold process demanding multifaceted models of neurocognitive ageing. Behavioural tests of executive functions are likely to share certain cognitive components, and are generally positively correlated[14] They represent a valuable avenue of insight into models of age-related changes in executive function: They allow for comparison of single versus multifactorial models, and an examination of distinct contributions of different neural properties of the frontal lobe. Our goal here is not to exhaustively cover the domain of executive functions, but instead to focus on two specific tests that are likely to measure dissociable executive functions (fluid intelligence and multi-tasking)—to put to test the prevalent unidimensional theories of executive function in ageing

Objectives

Methods

Results

Conclusion