Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing

The legalization of recreational cannabis use has expanded the availability of this psychoactive substance in the United States. Research has shown that chronic cannabis use is associated with altered working memory function, however, the brain areas and neural dynamics underlying these affects rema...

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Main Authors: Peihan J. Huang, Jake J. Son, Yasra Arif, Jason A. John, Lucy K. Horne, Mikki Schantell, Seth D. Springer, Maggie P. Rempe, Hannah J. Okelberry, Abraham D. Killanin, Ryan Glesinger, Anna T. Coutant, Thomas W. Ward, Madelyn P. Willett, Hallie J. Johnson, Elizabeth Heinrichs-Graham, Tony W. Wilson
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Neurobiology of Disease
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Online Access:http://www.sciencedirect.com/science/article/pii/S0969996125000087
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author Peihan J. Huang
Jake J. Son
Yasra Arif
Jason A. John
Lucy K. Horne
Mikki Schantell
Seth D. Springer
Maggie P. Rempe
Hannah J. Okelberry
Abraham D. Killanin
Ryan Glesinger
Anna T. Coutant
Thomas W. Ward
Madelyn P. Willett
Hallie J. Johnson
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_facet Peihan J. Huang
Jake J. Son
Yasra Arif
Jason A. John
Lucy K. Horne
Mikki Schantell
Seth D. Springer
Maggie P. Rempe
Hannah J. Okelberry
Abraham D. Killanin
Ryan Glesinger
Anna T. Coutant
Thomas W. Ward
Madelyn P. Willett
Hallie J. Johnson
Elizabeth Heinrichs-Graham
Tony W. Wilson
author_sort Peihan J. Huang
collection DOAJ
description The legalization of recreational cannabis use has expanded the availability of this psychoactive substance in the United States. Research has shown that chronic cannabis use is associated with altered working memory function, however, the brain areas and neural dynamics underlying these affects remain poorly understood. In this study, we leveraged magnetoencephalography (MEG) to investigate neurophysiological activity in 45 participants (22 heavy cannabis users) during a numerical WM task, whereby participants were asked to either maintain or manipulate (i.e., rearrange in ascending order) a group of visually presented numbers. Significant oscillatory responses were imaged using a beamformer and subjected to whole-brain ANOVAs. Notably, we found that cannabis users exhibited significantly weaker alpha oscillations in superior parietal, occipital, and other regions during the encoding phase relative to nonusers. Interestingly, during the maintenance phase, there was a group-by-condition interaction in the right inferior frontal gyrus, left prefrontal, parietal, and other regions, such that cannabis users exhibited weaker alpha and beta oscillations relative to nonusers during maintain trials. Additionally, chronic cannabis users exhibited stronger alpha and beta maintenance responses in these same brain regions and prolonged reaction times during manipulate relative to maintain trials, while no such differences were found in nonusers. Neurobehavioral relationships were also detected in the prefrontal cortices of nonusers, but not cannabis users. In sum, chronic cannabis users exhibit weaker neural oscillations during working memory encoding but may compensate for these deficiencies through stronger oscillatory responses during memory maintenance, especially during strenuous tasks such as manipulating the to-be remembered items.
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spelling doaj-art-c92d698fda0f49939494bb947490e4252025-01-24T04:44:42ZengElsevierNeurobiology of Disease1095-953X2025-02-01205106792Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processingPeihan J. Huang0Jake J. Son1Yasra Arif2Jason A. John3Lucy K. Horne4Mikki Schantell5Seth D. Springer6Maggie P. Rempe7Hannah J. Okelberry8Abraham D. Killanin9Ryan Glesinger10Anna T. Coutant11Thomas W. Ward12Madelyn P. Willett13Hallie J. Johnson14Elizabeth Heinrichs-Graham15Tony W. Wilson16Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USAInstitute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USA; College of Medicine, University of Nebraska Medical Center (UNMC), Omaha, NE, USA; Corresponding author at: Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA.The legalization of recreational cannabis use has expanded the availability of this psychoactive substance in the United States. Research has shown that chronic cannabis use is associated with altered working memory function, however, the brain areas and neural dynamics underlying these affects remain poorly understood. In this study, we leveraged magnetoencephalography (MEG) to investigate neurophysiological activity in 45 participants (22 heavy cannabis users) during a numerical WM task, whereby participants were asked to either maintain or manipulate (i.e., rearrange in ascending order) a group of visually presented numbers. Significant oscillatory responses were imaged using a beamformer and subjected to whole-brain ANOVAs. Notably, we found that cannabis users exhibited significantly weaker alpha oscillations in superior parietal, occipital, and other regions during the encoding phase relative to nonusers. Interestingly, during the maintenance phase, there was a group-by-condition interaction in the right inferior frontal gyrus, left prefrontal, parietal, and other regions, such that cannabis users exhibited weaker alpha and beta oscillations relative to nonusers during maintain trials. Additionally, chronic cannabis users exhibited stronger alpha and beta maintenance responses in these same brain regions and prolonged reaction times during manipulate relative to maintain trials, while no such differences were found in nonusers. Neurobehavioral relationships were also detected in the prefrontal cortices of nonusers, but not cannabis users. In sum, chronic cannabis users exhibit weaker neural oscillations during working memory encoding but may compensate for these deficiencies through stronger oscillatory responses during memory maintenance, especially during strenuous tasks such as manipulating the to-be remembered items.http://www.sciencedirect.com/science/article/pii/S0969996125000087MagnetoencephalographyMEGMarijuanaSubstance usecannabis use disorderShort-term memory
spellingShingle Peihan J. Huang
Jake J. Son
Yasra Arif
Jason A. John
Lucy K. Horne
Mikki Schantell
Seth D. Springer
Maggie P. Rempe
Hannah J. Okelberry
Abraham D. Killanin
Ryan Glesinger
Anna T. Coutant
Thomas W. Ward
Madelyn P. Willett
Hallie J. Johnson
Elizabeth Heinrichs-Graham
Tony W. Wilson
Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
Neurobiology of Disease
Magnetoencephalography
MEG
Marijuana
Substance use
cannabis use disorder
Short-term memory
title Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
title_full Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
title_fullStr Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
title_full_unstemmed Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
title_short Chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
title_sort chronic cannabis use differentially modulates neural oscillations serving the manipulate versus maintain components of working memory processing
topic Magnetoencephalography
MEG
Marijuana
Substance use
cannabis use disorder
Short-term memory
url http://www.sciencedirect.com/science/article/pii/S0969996125000087
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