Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity

Dávid Samu; Karen L. Campbell; Kamen A. Tsvetanov; Meredith A. Shafto; Carol Brayne; Edward T. Bullmore; Andrew C. Calder; Rhodri Cusack; Tim Dalgleish; John Duncan; Richard N. Henson; Fiona E. Matthews; William D. Marslen-Wilson; James B. Rowe; Teresa Cheung; Simon Davis; Linda Geerligs; Rogier Kievit; Anna McCarrey; Abdur Mustafa; Darren Price; Jason R. Taylor; Matthias Treder; Janna Van Belle; Nitin Williams; Lauren Bates; Tina Emery; Sharon Erzinclioglu; Andrew Gadie; Sofia Gerbase; Stanimira Georgieva; Claire Hanley; Beth Parkin; David Troy; Tibor Auer; Marta Correia; Lu Gao; Emma Green; Rafael Henriques; Jodie Allen; Gillian Amery; Liana Amunts; Anne Barcroft; Amanda Castle; Cheryl DIas; Jonathan Dowrick; Melissa Fair; Hayley Fisher; Anna Goulding; Adarsh Grewal; Geoff Hale; Andrew Hilton; Frances Johnson; Patricia Johnston; Thea Kavanagh-Williamson; Magdalena Kwasniewska; Alison McMinn; Kim Norman; Jessica Penrose; Fiona Roby; DIane Rowland; John Sargeant; Maggie Squire; Beth Stevens; Aldabra Stoddart; Cheryl Stone; Tracy Thompson; Ozlem Yazlik; Dan Barnes; Marie DIxon; Jaya Hillman; Joanne Mitchell; Laura Villis; Lorraine K. Tyler

doi:10.1038/ncomms14743

Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity

Dávid Samu^*, Karen L. Campbell, Kamen A. Tsvetanov, Meredith A. Shafto, Carol Brayne, Edward T. Bullmore, Andrew C. Calder, Rhodri Cusack, Tim Dalgleish, John Duncan, Richard N. Henson, Fiona E. Matthews, William D. Marslen-Wilson, James B. Rowe, Teresa Cheung, Simon Davis, Linda Geerligs, Rogier Kievit, Anna McCarrey, Abdur MustafaDarren Price, Jason R. Taylor, Matthias Treder, Janna Van Belle, Nitin Williams, Lauren Bates, Tina Emery, Sharon Erzinclioglu, Andrew Gadie, Sofia Gerbase, Stanimira Georgieva, Claire Hanley, Beth Parkin, David Troy, Tibor Auer, Marta Correia, Lu Gao, Emma Green, Rafael Henriques, Jodie Allen, Gillian Amery, Liana Amunts, Anne Barcroft, Amanda Castle, Cheryl DIas, Jonathan Dowrick, Melissa Fair, Hayley Fisher, Anna Goulding, Adarsh Grewal, Geoff Hale, Andrew Hilton, Frances Johnson, Patricia Johnston, Thea Kavanagh-Williamson, Magdalena Kwasniewska, Alison McMinn, Kim Norman, Jessica Penrose, Fiona Roby, DIane Rowland, John Sargeant, Maggie Squire, Beth Stevens, Aldabra Stoddart, Cheryl Stone, Tracy Thompson, Ozlem Yazlik, Dan Barnes, Marie DIxon, Jaya Hillman, Joanne Mitchell, Laura Villis, Lorraine K. Tyler

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Healthy ageing has disparate effects on different cognitive domains. The neural basis of these differences, however, is largely unknown. We investigated this question by using Independent Components Analysis to obtain functional brain components from 98 healthy participants aged 23-87 years from the population-based Cam-CAN cohort. Participants performed two cognitive tasks that show age-related decrease (fluid intelligence and object naming) and a syntactic comprehension task that shows age-related preservation. We report that activation of task-positive neural components predicts inter-individual differences in performance in each task across the adult lifespan. Furthermore, only the two tasks that show performance declines with age show age-related decreases in task-positive activation of neural components and decreasing default mode (DM) suppression. Our results suggest that distributed, multi-component brain responsivity supports cognition across the adult lifespan, and the maintenance of this, along with maintained DM deactivation, characterizes successful ageing and may explain differential ageing trajectories across cognitive domains.

Original language	English
Article number	14743
Journal	Nature Communications
Volume	8
DOIs	https://doi.org/10.1038/ncomms14743
State	Published - 8 May 2017
Externally published	Yes

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Samu, D., Campbell, K. L., Tsvetanov, K. A., Shafto, M. A., Brayne, C., Bullmore, E. T., Calder, A. C., Cusack, R., Dalgleish, T., Duncan, J., Henson, R. N., Matthews, F. E., Marslen-Wilson, W. D., Rowe, J. B., Cheung, T., Davis, S., Geerligs, L., Kievit, R., McCarrey, A., ... Tyler, L. K. (2017). Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity. Nature Communications, 8, Article 14743. https://doi.org/10.1038/ncomms14743

@article{24268bba44a34558abf8bcb4bf0f9579,

title = "Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity",

abstract = "Healthy ageing has disparate effects on different cognitive domains. The neural basis of these differences, however, is largely unknown. We investigated this question by using Independent Components Analysis to obtain functional brain components from 98 healthy participants aged 23-87 years from the population-based Cam-CAN cohort. Participants performed two cognitive tasks that show age-related decrease (fluid intelligence and object naming) and a syntactic comprehension task that shows age-related preservation. We report that activation of task-positive neural components predicts inter-individual differences in performance in each task across the adult lifespan. Furthermore, only the two tasks that show performance declines with age show age-related decreases in task-positive activation of neural components and decreasing default mode (DM) suppression. Our results suggest that distributed, multi-component brain responsivity supports cognition across the adult lifespan, and the maintenance of this, along with maintained DM deactivation, characterizes successful ageing and may explain differential ageing trajectories across cognitive domains.",

author = "D{\'a}vid Samu and Campbell, {Karen L.} and Tsvetanov, {Kamen A.} and Shafto, {Meredith A.} and Carol Brayne and Bullmore, {Edward T.} and Calder, {Andrew C.} and Rhodri Cusack and Tim Dalgleish and John Duncan and Henson, {Richard N.} and Matthews, {Fiona E.} and Marslen-Wilson, {William D.} and Rowe, {James B.} and Teresa Cheung and Simon Davis and Linda Geerligs and Rogier Kievit and Anna McCarrey and Abdur Mustafa and Darren Price and Taylor, {Jason R.} and Matthias Treder and {Van Belle}, Janna and Nitin Williams and Lauren Bates and Tina Emery and Sharon Erzinclioglu and Andrew Gadie and Sofia Gerbase and Stanimira Georgieva and Claire Hanley and Beth Parkin and David Troy and Tibor Auer and Marta Correia and Lu Gao and Emma Green and Rafael Henriques and Jodie Allen and Gillian Amery and Liana Amunts and Anne Barcroft and Amanda Castle and Cheryl DIas and Jonathan Dowrick and Melissa Fair and Hayley Fisher and Anna Goulding and Adarsh Grewal and Geoff Hale and Andrew Hilton and Frances Johnson and Patricia Johnston and Thea Kavanagh-Williamson and Magdalena Kwasniewska and Alison McMinn and Kim Norman and Jessica Penrose and Fiona Roby and DIane Rowland and John Sargeant and Maggie Squire and Beth Stevens and Aldabra Stoddart and Cheryl Stone and Tracy Thompson and Ozlem Yazlik and Dan Barnes and Marie DIxon and Jaya Hillman and Joanne Mitchell and Laura Villis and Tyler, {Lorraine K.}",

note = "Publisher Copyright: {\textcopyright} 2017 The Author(s).",

year = "2017",

month = may,

day = "8",

doi = "10.1038/ncomms14743",

language = "אנגלית",

volume = "8",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

}

Samu, D, Campbell, KL, Tsvetanov, KA, Shafto, MA, Brayne, C, Bullmore, ET, Calder, AC, Cusack, R, Dalgleish, T, Duncan, J, Henson, RN, Matthews, FE, Marslen-Wilson, WD, Rowe, JB, Cheung, T, Davis, S, Geerligs, L, Kievit, R, McCarrey, A, Mustafa, A, Price, D, Taylor, JR, Treder, M, Van Belle, J, Williams, N, Bates, L, Emery, T, Erzinclioglu, S, Gadie, A, Gerbase, S, Georgieva, S, Hanley, C, Parkin, B, Troy, D, Auer, T, Correia, M, Gao, L, Green, E, Henriques, R, Allen, J, Amery, G, Amunts, L, Barcroft, A, Castle, A, DIas, C, Dowrick, J, Fair, M, Fisher, H, Goulding, A, Grewal, A, Hale, G, Hilton, A, Johnson, F, Johnston, P, Kavanagh-Williamson, T, Kwasniewska, M, McMinn, A, Norman, K, Penrose, J, Roby, F, Rowland, DI, Sargeant, J, Squire, M, Stevens, B, Stoddart, A, Stone, C, Thompson, T, Yazlik, O, Barnes, D, DIxon, M, Hillman, J, Mitchell, J, Villis, L & Tyler, LK 2017, 'Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity', Nature Communications, vol. 8, 14743. https://doi.org/10.1038/ncomms14743

TY - JOUR

T1 - Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity

AU - Samu, Dávid

AU - Campbell, Karen L.

AU - Tsvetanov, Kamen A.

AU - Shafto, Meredith A.

AU - Brayne, Carol

AU - Bullmore, Edward T.

AU - Calder, Andrew C.

AU - Cusack, Rhodri

AU - Dalgleish, Tim

AU - Duncan, John

AU - Henson, Richard N.

AU - Matthews, Fiona E.

AU - Marslen-Wilson, William D.

AU - Rowe, James B.

AU - Cheung, Teresa

AU - Davis, Simon

AU - Geerligs, Linda

AU - Kievit, Rogier

AU - McCarrey, Anna

AU - Mustafa, Abdur

AU - Price, Darren

AU - Taylor, Jason R.

AU - Treder, Matthias

AU - Van Belle, Janna

AU - Williams, Nitin

AU - Bates, Lauren

AU - Emery, Tina

AU - Erzinclioglu, Sharon

AU - Gadie, Andrew

AU - Gerbase, Sofia

AU - Georgieva, Stanimira

AU - Hanley, Claire

AU - Parkin, Beth

AU - Troy, David

AU - Auer, Tibor

AU - Correia, Marta

AU - Gao, Lu

AU - Green, Emma

AU - Henriques, Rafael

AU - Allen, Jodie

AU - Amery, Gillian

AU - Amunts, Liana

AU - Barcroft, Anne

AU - Castle, Amanda

AU - DIas, Cheryl

AU - Dowrick, Jonathan

AU - Fair, Melissa

AU - Fisher, Hayley

AU - Goulding, Anna

AU - Grewal, Adarsh

AU - Hale, Geoff

AU - Hilton, Andrew

AU - Johnson, Frances

AU - Johnston, Patricia

AU - Kavanagh-Williamson, Thea

AU - Kwasniewska, Magdalena

AU - McMinn, Alison

AU - Norman, Kim

AU - Penrose, Jessica

AU - Roby, Fiona

AU - Rowland, DIane

AU - Sargeant, John

AU - Squire, Maggie

AU - Stevens, Beth

AU - Stoddart, Aldabra

AU - Stone, Cheryl

AU - Thompson, Tracy

AU - Yazlik, Ozlem

AU - Barnes, Dan

AU - DIxon, Marie

AU - Hillman, Jaya

AU - Mitchell, Joanne

AU - Villis, Laura

AU - Tyler, Lorraine K.

PY - 2017/5/8

Y1 - 2017/5/8

N2 - Healthy ageing has disparate effects on different cognitive domains. The neural basis of these differences, however, is largely unknown. We investigated this question by using Independent Components Analysis to obtain functional brain components from 98 healthy participants aged 23-87 years from the population-based Cam-CAN cohort. Participants performed two cognitive tasks that show age-related decrease (fluid intelligence and object naming) and a syntactic comprehension task that shows age-related preservation. We report that activation of task-positive neural components predicts inter-individual differences in performance in each task across the adult lifespan. Furthermore, only the two tasks that show performance declines with age show age-related decreases in task-positive activation of neural components and decreasing default mode (DM) suppression. Our results suggest that distributed, multi-component brain responsivity supports cognition across the adult lifespan, and the maintenance of this, along with maintained DM deactivation, characterizes successful ageing and may explain differential ageing trajectories across cognitive domains.

AB - Healthy ageing has disparate effects on different cognitive domains. The neural basis of these differences, however, is largely unknown. We investigated this question by using Independent Components Analysis to obtain functional brain components from 98 healthy participants aged 23-87 years from the population-based Cam-CAN cohort. Participants performed two cognitive tasks that show age-related decrease (fluid intelligence and object naming) and a syntactic comprehension task that shows age-related preservation. We report that activation of task-positive neural components predicts inter-individual differences in performance in each task across the adult lifespan. Furthermore, only the two tasks that show performance declines with age show age-related decreases in task-positive activation of neural components and decreasing default mode (DM) suppression. Our results suggest that distributed, multi-component brain responsivity supports cognition across the adult lifespan, and the maintenance of this, along with maintained DM deactivation, characterizes successful ageing and may explain differential ageing trajectories across cognitive domains.

UR - http://www.scopus.com/inward/record.url?scp=85019080143&partnerID=8YFLogxK

U2 - 10.1038/ncomms14743

DO - 10.1038/ncomms14743

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

C2 - 28480894

AN - SCOPUS:85019080143

SN - 2041-1723

VL - 8

JO - Nature Communications

JF - Nature Communications

M1 - 14743

ER -

Preserved cognitive functions with age are determined by domain-dependent shifts in network responsivity

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