Idiosyncratic responding during movie-watching predicted by age differences in attentional control

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

doi:10.1016/j.neurobiolaging.2015.07.028

Abstract

Much is known about how age affects the brain during tightly controlled, though largely contrived, experiments, but do these effects extrapolate to everyday life? Naturalistic stimuli, such as movies, closely mimic the real world and provide a window onto the brain's ability to respond in a timely and measured fashion to complex, everyday events. Young adults respond to these stimuli in a highly synchronized fashion, but it remains to be seen how age affects neural responsiveness during naturalistic viewing. To this end, we scanned a large (N = 218), population-based sample from the Cambridge Centre for Ageing and Neuroscience (Cam-CAN) during movie-watching. Intersubject synchronization declined with age, such that older adults' response to the movie was more idiosyncratic. This decreased synchrony related to cognitive measures sensitive to attentional control. Our findings suggest that neural responsivity changes with age, which likely has important implications for real-world event comprehension and memory.

Highlights

Movies have the power to transport your mind from the narrow, impersonal bore of an magnetic resonance imaging (MRI) magnet to a world more synonymous with everyday life, replete with sights, sounds, and language
We expected intersubject synchronization to be positively related to measures which are sensitive to attentional control
Participants performed several cognitive tasks outside the scanner as part of a larger test battery, but here, we focus on measures which are sensitive to attentional control and control measures which are less dependent on control

Summary

Introduction

Movies have the power to transport your mind from the narrow, impersonal bore of an magnetic resonance imaging (MRI) magnet to a world more synonymous with everyday life, replete with sights, sounds, and language Despite their complexity, these naturalistic stimuli tend to drive neural activation in the same way across individuals (Hasson et al, 2004, 2010), suggesting that our experience of real-world events is largely shared. Responding in the same way as others is not a perquisite for perception, it does seem to reflect the optimal response to a given stimulus, in that asynchronous responding tends to relate to poor comprehension (Hasson et al, 2009) and memory (Hasson et al, 2008a) This may be because synchronized activity reflects shared attention to the most relevant stimulus in the environment, as nominated by the majority. Individuals with greater attentional control should be better able to maintain focus on the movie and should show higher synchronization with others

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Results

Conclusion