Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance

Numerous investigations have characterized the oscillatory dynamics serving working memory in adults, but few have probed its relationship with chronological age in developing youth. We recorded magnetoencephalography during a modified Sternberg verbal working memory task in 82 youth participants ag...

Full description

Bibliographic Details
Main Authors: Abraham D. Killanin, Thomas W. Ward, Christine M. Embury, Vince D. Calhoun, Yu-Ping Wang, Julia M. Stephen, Giorgia Picci, Elizabeth Heinrichs-Graham, Tony W. Wilson
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:Developmental Cognitive Neuroscience
Online Access:http://www.sciencedirect.com/science/article/pii/S187892932400015X
_version_ 1797198762914873344
author Abraham D. Killanin
Thomas W. Ward
Christine M. Embury
Vince D. Calhoun
Yu-Ping Wang
Julia M. Stephen
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_facet Abraham D. Killanin
Thomas W. Ward
Christine M. Embury
Vince D. Calhoun
Yu-Ping Wang
Julia M. Stephen
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_sort Abraham D. Killanin
collection DOAJ
description Numerous investigations have characterized the oscillatory dynamics serving working memory in adults, but few have probed its relationship with chronological age in developing youth. We recorded magnetoencephalography during a modified Sternberg verbal working memory task in 82 youth participants aged 6–14 years old. Significant oscillatory responses were identified and imaged using a beamforming approach and the resulting whole-brain maps were probed for developmental effects during the encoding and maintenance phases. Our results indicated robust oscillatory responses in the theta (4–7 Hz) and alpha (8–14 Hz) range, with older participants exhibiting stronger alpha oscillations in left-hemispheric language regions. Older participants also had greater occipital theta power during encoding. Interestingly, there were sex-by-age interaction effects in cerebellar cortices during encoding and in the right superior temporal region during maintenance. These results extend the existing literature on working memory development by showing strong associations between age and oscillatory dynamics across a distributed network. To our knowledge, these findings are the first to link chronological age to alpha and theta oscillatory responses serving working memory encoding and maintenance, both across and between male and female youth; they reveal robust developmental effects in crucial brain regions serving higher order functions.
first_indexed 2024-03-08T04:50:21Z
format Article
id doaj.art-11fc0a6ba9b348d9864596130e577813
institution Directory Open Access Journal
issn 1878-9293
language English
last_indexed 2024-04-24T07:05:01Z
publishDate 2024-04-01
publisher Elsevier
record_format Article
series Developmental Cognitive Neuroscience
spelling doaj.art-11fc0a6ba9b348d9864596130e5778132024-04-22T04:11:34ZengElsevierDevelopmental Cognitive Neuroscience1878-92932024-04-0166101354Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenanceAbraham D. Killanin0Thomas W. Ward1Christine M. Embury2Vince D. Calhoun3Yu-Ping Wang4Julia M. Stephen5Giorgia Picci6Elizabeth Heinrichs-Graham7Tony W. Wilson8Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology and Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USATri-Institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, and Emory University, Atlanta, GA, USADepartment of Biomedical Engineering, Tulane University, New Orleans, LA, USAMind Research Network, Albuquerque, NM, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology and Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology and Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA; Department of Pharmacology and Neuroscience, Creighton University, Omaha, NE, USA; Correspondence to: Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE 68010, USA.Numerous investigations have characterized the oscillatory dynamics serving working memory in adults, but few have probed its relationship with chronological age in developing youth. We recorded magnetoencephalography during a modified Sternberg verbal working memory task in 82 youth participants aged 6–14 years old. Significant oscillatory responses were identified and imaged using a beamforming approach and the resulting whole-brain maps were probed for developmental effects during the encoding and maintenance phases. Our results indicated robust oscillatory responses in the theta (4–7 Hz) and alpha (8–14 Hz) range, with older participants exhibiting stronger alpha oscillations in left-hemispheric language regions. Older participants also had greater occipital theta power during encoding. Interestingly, there were sex-by-age interaction effects in cerebellar cortices during encoding and in the right superior temporal region during maintenance. These results extend the existing literature on working memory development by showing strong associations between age and oscillatory dynamics across a distributed network. To our knowledge, these findings are the first to link chronological age to alpha and theta oscillatory responses serving working memory encoding and maintenance, both across and between male and female youth; they reveal robust developmental effects in crucial brain regions serving higher order functions.http://www.sciencedirect.com/science/article/pii/S187892932400015X
spellingShingle Abraham D. Killanin
Thomas W. Ward
Christine M. Embury
Vince D. Calhoun
Yu-Ping Wang
Julia M. Stephen
Giorgia Picci
Elizabeth Heinrichs-Graham
Tony W. Wilson
Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
Developmental Cognitive Neuroscience
title Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
title_full Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
title_fullStr Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
title_full_unstemmed Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
title_short Better with age: Developmental changes in oscillatory activity during verbal working memory encoding and maintenance
title_sort better with age developmental changes in oscillatory activity during verbal working memory encoding and maintenance
url http://www.sciencedirect.com/science/article/pii/S187892932400015X
work_keys_str_mv AT abrahamdkillanin betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT thomaswward betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT christinemembury betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT vincedcalhoun betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT yupingwang betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT juliamstephen betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT giorgiapicci betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT elizabethheinrichsgraham betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance
AT tonywwilson betterwithagedevelopmentalchangesinoscillatoryactivityduringverbalworkingmemoryencodingandmaintenance