White matter hyperintensities among older adults are associated with futile increase in frontal activation and functional connectivity during spatial search

Samuel N. Lockhart, Steven J. Luck, Joy Geng, Laurel A Beckett, Elizabeth A. Disbrow, Owen Carmichael, Charles DeCarli

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

The mechanisms by which aging and other processes can affect the structure and function of brain networks are important to understanding normal age-related cognitive decline. Advancing age is known to be associated with various disease processes, including clinically asymptomatic vascular and inflammation processes that contribute to white matter structural alteration and potential injury. The effects of these processes on the function of distributed cognitive networks, however, are poorly understood. We hypothesized that the extent of magnetic resonance imaging white matter hyperintensities would be associated with visual attentional control in healthy aging, measured using a functional magnetic resonance imaging search task. We assessed cognitively healthy older adults with search tasks indexing processing speed and attentional control. Expanding upon previous research, older adults demonstrate activation across a frontal-parietal attentional control network. Further, greater white matter hyperintensity volume was associated with increased activation of a frontal network node independent of chronological age. Also consistent with previous research, greater white matter hyperintensity volume was associated with anatomically specific reductions in functional magnetic resonance imaging functional connectivity during search among attentional control regions. White matter hyperintensities may lead to subtle attentional network dysfunction, potentially through impaired frontal-parietal and frontal interhemispheric connectivity, suggesting that clinically silent white matter biomarkers of vascular and inflammatory injury can contribute to differences in search performance and brain function in aging, and likely contribute to advanced age-related impairments in cognitive control.

Original languageEnglish (US)
Article numbere0122445
JournalPLoS One
Volume10
Issue number3
DOIs
StatePublished - Mar 20 2015

Fingerprint

magnetic resonance imaging
Chemical activation
blood vessels
Aging of materials
brain
Magnetic Resonance Imaging
Brain
cognition
biomarkers
inflammation
Biomarkers
Magnetic resonance
Vascular System Injuries
Research
Cognition
Blood Vessels
White Matter
Imaging techniques
Inflammation
Processing

ASJC Scopus subject areas

  • Medicine(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

White matter hyperintensities among older adults are associated with futile increase in frontal activation and functional connectivity during spatial search. / Lockhart, Samuel N.; Luck, Steven J.; Geng, Joy; Beckett, Laurel A; Disbrow, Elizabeth A.; Carmichael, Owen; DeCarli, Charles.

In: PLoS One, Vol. 10, No. 3, e0122445, 20.03.2015.

Research output: Contribution to journalArticle

@article{c216720980a04610b067ea6c4f613483,
title = "White matter hyperintensities among older adults are associated with futile increase in frontal activation and functional connectivity during spatial search",
abstract = "The mechanisms by which aging and other processes can affect the structure and function of brain networks are important to understanding normal age-related cognitive decline. Advancing age is known to be associated with various disease processes, including clinically asymptomatic vascular and inflammation processes that contribute to white matter structural alteration and potential injury. The effects of these processes on the function of distributed cognitive networks, however, are poorly understood. We hypothesized that the extent of magnetic resonance imaging white matter hyperintensities would be associated with visual attentional control in healthy aging, measured using a functional magnetic resonance imaging search task. We assessed cognitively healthy older adults with search tasks indexing processing speed and attentional control. Expanding upon previous research, older adults demonstrate activation across a frontal-parietal attentional control network. Further, greater white matter hyperintensity volume was associated with increased activation of a frontal network node independent of chronological age. Also consistent with previous research, greater white matter hyperintensity volume was associated with anatomically specific reductions in functional magnetic resonance imaging functional connectivity during search among attentional control regions. White matter hyperintensities may lead to subtle attentional network dysfunction, potentially through impaired frontal-parietal and frontal interhemispheric connectivity, suggesting that clinically silent white matter biomarkers of vascular and inflammatory injury can contribute to differences in search performance and brain function in aging, and likely contribute to advanced age-related impairments in cognitive control.",
author = "Lockhart, {Samuel N.} and Luck, {Steven J.} and Joy Geng and Beckett, {Laurel A} and Disbrow, {Elizabeth A.} and Owen Carmichael and Charles DeCarli",
year = "2015",
month = "3",
day = "20",
doi = "10.1371/journal.pone.0122445",
language = "English (US)",
volume = "10",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "3",

}

TY - JOUR

T1 - White matter hyperintensities among older adults are associated with futile increase in frontal activation and functional connectivity during spatial search

AU - Lockhart, Samuel N.

AU - Luck, Steven J.

AU - Geng, Joy

AU - Beckett, Laurel A

AU - Disbrow, Elizabeth A.

AU - Carmichael, Owen

AU - DeCarli, Charles

PY - 2015/3/20

Y1 - 2015/3/20

N2 - The mechanisms by which aging and other processes can affect the structure and function of brain networks are important to understanding normal age-related cognitive decline. Advancing age is known to be associated with various disease processes, including clinically asymptomatic vascular and inflammation processes that contribute to white matter structural alteration and potential injury. The effects of these processes on the function of distributed cognitive networks, however, are poorly understood. We hypothesized that the extent of magnetic resonance imaging white matter hyperintensities would be associated with visual attentional control in healthy aging, measured using a functional magnetic resonance imaging search task. We assessed cognitively healthy older adults with search tasks indexing processing speed and attentional control. Expanding upon previous research, older adults demonstrate activation across a frontal-parietal attentional control network. Further, greater white matter hyperintensity volume was associated with increased activation of a frontal network node independent of chronological age. Also consistent with previous research, greater white matter hyperintensity volume was associated with anatomically specific reductions in functional magnetic resonance imaging functional connectivity during search among attentional control regions. White matter hyperintensities may lead to subtle attentional network dysfunction, potentially through impaired frontal-parietal and frontal interhemispheric connectivity, suggesting that clinically silent white matter biomarkers of vascular and inflammatory injury can contribute to differences in search performance and brain function in aging, and likely contribute to advanced age-related impairments in cognitive control.

AB - The mechanisms by which aging and other processes can affect the structure and function of brain networks are important to understanding normal age-related cognitive decline. Advancing age is known to be associated with various disease processes, including clinically asymptomatic vascular and inflammation processes that contribute to white matter structural alteration and potential injury. The effects of these processes on the function of distributed cognitive networks, however, are poorly understood. We hypothesized that the extent of magnetic resonance imaging white matter hyperintensities would be associated with visual attentional control in healthy aging, measured using a functional magnetic resonance imaging search task. We assessed cognitively healthy older adults with search tasks indexing processing speed and attentional control. Expanding upon previous research, older adults demonstrate activation across a frontal-parietal attentional control network. Further, greater white matter hyperintensity volume was associated with increased activation of a frontal network node independent of chronological age. Also consistent with previous research, greater white matter hyperintensity volume was associated with anatomically specific reductions in functional magnetic resonance imaging functional connectivity during search among attentional control regions. White matter hyperintensities may lead to subtle attentional network dysfunction, potentially through impaired frontal-parietal and frontal interhemispheric connectivity, suggesting that clinically silent white matter biomarkers of vascular and inflammatory injury can contribute to differences in search performance and brain function in aging, and likely contribute to advanced age-related impairments in cognitive control.

UR - http://www.scopus.com/inward/record.url?scp=84961290675&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84961290675&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0122445

DO - 10.1371/journal.pone.0122445

M3 - Article

VL - 10

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 3

M1 - e0122445

ER -