Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning

BackgroundSelf-generation of material compared to passive learning results in mproved memory performance; this may be related to recruitment of a fronto-temporal encoding network. Using a verbal paired-associate learning fMRI task, we examined the effects of sex, age, and handedness on the neural co...

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Main Authors: Sangeeta Nair, Rodolphe E. Nenert, Jane B. Allendorfer, Adam M. Goodman, Jennifer Vannest, Daniel Mirman, Jerzy P. Szaflarski
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Neuroscience
Subjects:
sex
age
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.00961/full
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spelling doaj-2edd9f0cc2aa410f94a7994668a02fec2020-11-24T22:26:11ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-09-011310.3389/fnins.2019.00961449960Sex, Age, and Handedness Modulate the Neural Correlates of Active LearningSangeeta Nair0Sangeeta Nair1Rodolphe E. Nenert2Jane B. Allendorfer3Adam M. Goodman4Jennifer Vannest5Daniel Mirman6Jerzy P. Szaflarski7Department of Neurology, The University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Psychology, The University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, The University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, The University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, The University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Pediatrics, Division of Neurology, Cincinnati Children’s Hospital Medical Center, Pediatric Neuroimaging Research Consortium, University of Cincinnati College of Medicine, Cincinnati, OH, United StatesDepartment of Psychology, University of Edinburgh, Edinburgh, United KingdomDepartment of Neurology, The University of Alabama at Birmingham, Birmingham, AL, United StatesBackgroundSelf-generation of material compared to passive learning results in mproved memory performance; this may be related to recruitment of a fronto-temporal encoding network. Using a verbal paired-associate learning fMRI task, we examined the effects of sex, age, and handedness on the neural correlates of self-generation.MethodsData from 174 healthy English-speaking participants (78M, 56 atypically handed; ages 19–76) were preprocessed using AFNI and FSL. Independent component analysis was conducted using GIFT (Group ICA fMRI Toolbox). Forty-one independent components were temporally sorted by task time series. Retaining correlations (r > 0.25) resulted in three task-positive (“generate”) and three task-negative (“read”) components. Using participants’ back-projected components, we evaluated the effects of sex, handedness, and aging on activation lateralization and localization in task-relevant networks with two-sample t-tests. Further, we examined the linear relationship between sex and neuroimaging data with multiple regression, covarying for scanner, age, and handedness.ResultsTask-positive components identified using ICA revealed a fronto-parietal network involved with self-generation, while task-negative components reflecting passive reading showed temporo-occipital involvement. Compared to older adults, younger adults exhibited greater task-positive involvement of the left inferior frontal gyrus and insula, whereas older adults exhibited reduced prefrontal lateralization. Greater involvement of the left angular gyrus in task-positive encoding networks among right-handed individuals suggests the reliance on left dominant semantic processing areas may be modulated by handedness. Sex effects on task-related encoding networks while controlling for age and handedness suggest increased right hemisphere recruitment among males compared to females, specifically in the paracentral lobe during self-generation and the suparmarginal gyrus during passive reading.ImplicationsIdentified neuroimaging differences suggest that sex, age, and handedness are factors in the differential recruitment of encoding network regions for both passive and active learning.https://www.frontiersin.org/article/10.3389/fnins.2019.00961/fullassociate learningfMRIhandednesssexageverbal memory
collection DOAJ
language English
format Article
sources DOAJ
author Sangeeta Nair
Sangeeta Nair
Rodolphe E. Nenert
Jane B. Allendorfer
Adam M. Goodman
Jennifer Vannest
Daniel Mirman
Jerzy P. Szaflarski
spellingShingle Sangeeta Nair
Sangeeta Nair
Rodolphe E. Nenert
Jane B. Allendorfer
Adam M. Goodman
Jennifer Vannest
Daniel Mirman
Jerzy P. Szaflarski
Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
Frontiers in Neuroscience
associate learning
fMRI
handedness
sex
age
verbal memory
author_facet Sangeeta Nair
Sangeeta Nair
Rodolphe E. Nenert
Jane B. Allendorfer
Adam M. Goodman
Jennifer Vannest
Daniel Mirman
Jerzy P. Szaflarski
author_sort Sangeeta Nair
title Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
title_short Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
title_full Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
title_fullStr Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
title_full_unstemmed Sex, Age, and Handedness Modulate the Neural Correlates of Active Learning
title_sort sex, age, and handedness modulate the neural correlates of active learning
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2019-09-01
description BackgroundSelf-generation of material compared to passive learning results in mproved memory performance; this may be related to recruitment of a fronto-temporal encoding network. Using a verbal paired-associate learning fMRI task, we examined the effects of sex, age, and handedness on the neural correlates of self-generation.MethodsData from 174 healthy English-speaking participants (78M, 56 atypically handed; ages 19–76) were preprocessed using AFNI and FSL. Independent component analysis was conducted using GIFT (Group ICA fMRI Toolbox). Forty-one independent components were temporally sorted by task time series. Retaining correlations (r > 0.25) resulted in three task-positive (“generate”) and three task-negative (“read”) components. Using participants’ back-projected components, we evaluated the effects of sex, handedness, and aging on activation lateralization and localization in task-relevant networks with two-sample t-tests. Further, we examined the linear relationship between sex and neuroimaging data with multiple regression, covarying for scanner, age, and handedness.ResultsTask-positive components identified using ICA revealed a fronto-parietal network involved with self-generation, while task-negative components reflecting passive reading showed temporo-occipital involvement. Compared to older adults, younger adults exhibited greater task-positive involvement of the left inferior frontal gyrus and insula, whereas older adults exhibited reduced prefrontal lateralization. Greater involvement of the left angular gyrus in task-positive encoding networks among right-handed individuals suggests the reliance on left dominant semantic processing areas may be modulated by handedness. Sex effects on task-related encoding networks while controlling for age and handedness suggest increased right hemisphere recruitment among males compared to females, specifically in the paracentral lobe during self-generation and the suparmarginal gyrus during passive reading.ImplicationsIdentified neuroimaging differences suggest that sex, age, and handedness are factors in the differential recruitment of encoding network regions for both passive and active learning.
topic associate learning
fMRI
handedness
sex
age
verbal memory
url https://www.frontiersin.org/article/10.3389/fnins.2019.00961/full
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