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

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

doi:10.1016/j.neurobiolaging.2015.07.028

Cited by 84 publications

(112 citation statements)

References 61 publications

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“…Head motion was significantly lower during movie watching (Campbell et al, 2015) relative to resting state, SNG, and Cattell tasks ( F = 14.44, p < 0.001), which is consistent with previous reports showing that individuals are more compliant during movie watching (Vanderwal et al, 2015). Moreover, head motion across the three cognitive states (resting state, movie watching, and Cattell task) was highly correlated with head motion during SNG ( r = 0.81, p < 0.001) and did not interact with age ( F = 1.84, p = 0.139).…”

Section: Resultssupporting

confidence: 91%

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

et al. 2018

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Inhibitory control requires precise regulation of activity and connectivity within multiple brain networks. Previous studies have typically evaluated age-related changes in regional activity or changes in interregional interactions. Instead, we test the hypothesis that activity and connectivity make distinct, complementary contributions to performance across the life span and the maintenance of successful inhibitory control systems. A representative sample of healthy human adults in a large, population-based life span cohort performed an integrated Stop-Signal (SS)/No-Go task during functional magnetic resonance imaging (n = 119; age range, 18–88 years). Individual differences in inhibitory control were measured in terms of the SS reaction time (SSRT), using the blocked integration method. Linear models and independent components analysis revealed that individual differences in SSRT correlated with both activity and connectivity in a distributed inhibition network, comprising prefrontal, premotor, and motor regions. Importantly, this pattern was moderated by age, such that the association between inhibitory control and connectivity, but not activity, differed with age. Multivariate statistics and out-of-sample validation tests of multifactorial functional organization identified differential roles of activity and connectivity in determining an individual's SSRT across the life span. We propose that age-related differences in adaptive cognitive control are best characterized by the joint consideration of multifocal activity and connectivity within distributed brain networks. These insights may facilitate the development of new strategies to support cognitive ability in old age.SIGNIFICANCE STATEMENT The preservation of cognitive and motor control is crucial for maintaining well being across the life span. We show that such control is determined by both activity and connectivity within distributed brain networks. In a large, population-based cohort, we used a novel whole-brain multivariate approach to estimate the functional components of inhibitory control, in terms of their activity and connectivity. Both activity and connectivity in the inhibition network changed with age. But only the association between performance and connectivity, not activity, differed with age. The results suggest that adaptive control is best characterized by the joint consideration of multifocal activity and connectivity. These insights may facilitate the development of new strategies to maintain cognitive ability across the life span in health and disease.

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Section: Resultssupporting

confidence: 91%

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

et al. 2018

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“…A well‐suited paradigm for this purpose is the viewing of a naturalistic movie (Campbell et al, 2015; Hasson, Malach, & Heeger, 2010). By correlating a given regional time course of activity across subjects, a measure of response homogeneity can be obtained.…”

Section: Introductionmentioning

confidence: 99%

“…A well-suited paradigm for this purpose is the viewing of a naturalistic movie (Campbell et al, 2015;Hasson, Malach, & Heeger, 2010).…”

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confidence: 99%

Brain dynamics in ASD during movie‐watching show idiosyncratic functional integration and segregation

Bolton

Jochaut

Giraud

et al. 2018

Human Brain Mapping

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To refine our understanding of autism spectrum disorders (ASD), studies of the brain in dynamic, multimodal and ecological experimental settings are required. One way to achieve this is to compare the neural responses of ASD and typically developing (TD) individuals when viewing a naturalistic movie, but the temporal complexity of the stimulus hampers this task, and the presence of intrinsic functional connectivity (FC) may overshadow movie‐driven fluctuations. Here, we detected inter‐subject functional correlation (ISFC) transients to disentangle movie‐induced functional changes from underlying resting‐state activity while probing FC dynamically. When considering the number of significant ISFC excursions triggered by the movie across the brain, connections between remote functional modules were more heterogeneously engaged in the ASD population. Dynamically tracking the temporal profiles of those ISFC changes and tying them to specific movie subparts, this idiosyncrasy in ASD responses was then shown to involve functional integration and segregation mechanisms such as response inhibition, background suppression, or multisensory integration, while low‐level visual processing was spared. Through the application of a new framework for the study of dynamic experimental paradigms, our results reveal a temporally localized idiosyncrasy in ASD responses, specific to short‐lived episodes of long‐range functional interplays.

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“…First, resting state scans are relatively easy to obtain and particularly well suited to special populations, such as children and others who may have difficulty performing experimental tasks in the scanner. While it is debatable whether older individuals fall into this category, and recent work has shown that naturalistic viewing paradigms (such as movie-watching) may be better suited to special populations as they increase compliance and minimize head motion in the scanner (Vanderwal, Kelly, Eilbott, Mayes, & Castellanos, 2015; Campbell et al, 2015), resting state runs certainly minimize the demands placed on elderly participants. Further, because there is no specific task to perform at rest, group differences in functional connectivity are thought to reflect intrinsic or unbiased differences in underlying network organization, rather than group differences in response to the task itself (although this assumption will be called into question below).…”

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Ageing and the resting state: is cognition obsolete?

Campbell

Schacter

2016

Language, Cognition and Neuroscience

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Recent years have seen the rise in popularity of the resting state approach to neurocognitive aging, with many studies examining age differences in functional connectivity at rest and relating these differences to cognitive performance outside the scanner. There are many advantages to the resting state that likely contribute to its popularity and indeed, many insights have been gained from this work. However, there are also several limitations of the resting state approach that restrict its ability to contribute to the study of neurocognitive aging. In this opinion piece, we consider some of those limitations and argue that task-based studies are still essential to developing a mechanistic understanding of how age affects the brain in a cognitively relevant manner – a fundamental goal of neuroscientific research into aging.

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

Cited by 84 publications

References 61 publications

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

Brain dynamics in ASD during movie‐watching show idiosyncratic functional integration and segregation

Ageing and the resting state: is cognition obsolete?

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