Effects of endogenous testosterone on oscillatory activity during verbal working memory in youth

Author:

Killanin Abraham D.123,Ward Thomas W.124,Embury Christine M.12,Calhoun Vince D.5,Wang Yu‐Ping6,Stephen Julia M.7ORCID,Picci Giorgia124ORCID,Heinrichs‐Graham Elizabeth124,Wilson Tony W.1234ORCID

Affiliation:

1. Institute for Human Neuroscience Boys Town National Research Hospital Nebraska USA

2. Center for Pediatric Brain Health Boys Town National Research Hospital Nebraska USA

3. College of Medicine University of Nebraska Medical Center Omaha Nebraska USA

4. Department of Pharmacology and Neuroscience Creighton University Omaha Nebraska USA

5. Tri‐Institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) Georgia State University, Georgia Institute of Technology, and Emory University Atlanta Georgia USA

6. Department of Biomedical Engineering Tulane University New Orleans Louisiana USA

7. Mind Research Network Albuquerque New Mexico USA

Abstract

AbstractTestosterone levels sharply rise during the transition from childhood to adolescence and these changes are known to be associated with changes in human brain structure. During this same developmental window, there are also robust changes in the neural oscillatory dynamics serving verbal working memory processing. Surprisingly, whereas many studies have investigated the effects of chronological age on the neural oscillations supporting verbal working memory, none have probed the impact of endogenous testosterone levels during this developmental period. Using a sample of 89 youth aged 6–14 years‐old, we collected salivary testosterone samples and recorded magnetoencephalography during a modified Sternberg verbal working memory task. Significant oscillatory responses were identified and imaged using a beamforming approach and the resulting maps were subjected to whole‐brain ANCOVAs examining the effects of testosterone and sex, controlling for age, during verbal working memory encoding and maintenance. Our primary results indicated robust testosterone‐related effects in theta (4–7 Hz) and alpha (8–14 Hz) oscillatory activity, controlling for age. During encoding, females exhibited weaker theta oscillations than males in right cerebellar cortices and stronger alpha oscillations in left temporal cortices. During maintenance, youth with greater testosterone exhibited weaker alpha oscillations in right parahippocampal and cerebellar cortices, as well as regions across the left‐lateralized language network. These results extend the existing literature on the development of verbal working memory processing by showing region and sex‐specific effects of testosterone, and are the first results to link endogenous testosterone levels to the neural oscillatory activity serving verbal working memory, above and beyond the effects of chronological age.

Funder

National Science Foundation

National Institute of Mental Health

National Institute of General Medical Sciences

Publisher

Wiley

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