Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development

• Type of Material: Article
• Authors: Nathan M Petro, Boys Town National Research Hospital; Lauren R Ott, Boys Town National Research Hospital; Samntha H Penhale, Boys Town National Research Hospital; Maggie P Rempe, Boys Town National Research Hospital; Christine M Embury, Boys Town National Research Hospital; Giorgia Picci, Boys Town National Research Hospital; Yu-Ping Wang, Tulane University; Julia M Stephen, Mind Research Network; Vince Calhoun, Emory University; Tony W Wilson, Boys Town Natl Res Hosp
• Language: English
• Date: 2022-06-07
• Publisher: ACADEMIC PRESS INC ELSEVIER SCIENCE
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2022 The Authors. Published by Elsevier Inc.
• Final Published Version (URL): http://dx.doi.org/10.1016/j.neuroimage.2022.119337
• Title of Journal or Parent Work: NEUROIMAGE
• Volume: 258
• Start Page: 119337
• End Page: 119337
• Grant/Funding Information: This work was supported by the National Science Foundation (#1539067 to TWW, YPW, JMS, and VDC and #2112455 to VDC), the National Institutes of Health (R01-MH121101, R01-MH116782, R01-MH118013, and P20-GM144641 to TWW; R01-EB020407, R01-MH118695, and R01-MH123610 to VDC; R56-MH124925 to YPW). Funding agencies had no part in the study design or the writing of this report.
• Keywords: FUNCTIONAL CONNECTIVITY; OSCILLATIONS; ATTENTION-DEFICIT/HYPERACTIVITY DISORDER; Neurosciences; Neuroimaging; Oscillations; Beta; POWER; Science & Technology; Radiology, Nuclear Medicine & Medical Imaging; MEG; THETA-RHYTHM; EEG; Alpha; ALPHA-RHYTHM; Adolescence; ELECTROENCEPHALOGRAM; Life Sciences & Biomedicine; VISUAL-CORTEX; MAGNETOENCEPHALOGRAPHY; Neurosciences & Neurology; Magnetoencephalography; Resting state

Abstract

Background: Assessing brain activity during rest has become a widely used approach in developmental neuroscience. Extant literature has measured resting brain activity both during eyes-open and eyes-closed conditions, but the difference between these conditions has not yet been well characterized. Studies, limited to fMRI and EEG, have suggested that eyes-open versus -closed conditions may differentially impact neural activity, especially in visual cortices. Methods: Spontaneous cortical activity was recorded using MEG from 108 typically developing youth (9-15 years-old; 55 female) during separate sessions of eyes-open and eyes-closed rest. MEG source images were computed, and the strength of spontaneous neural activity was estimated in the canonical delta, theta, alpha, beta, and gamma bands, respectively. Power spectral density maps for eyes-open were subtracted from eyes-closed rest, and then submitted to vertex-wise regression models to identify spatially specific differences between conditions and as a function of age and sex. Results: Relative alpha power was weaker in the eyes-open compared to -closed condition, but otherwise eyes-open was stronger in all frequency bands, with differences concentrated in the occipital cortex. Relative theta power became stronger in the eyes-open compared to the eyes-closed condition with increasing age in frontal cortex. No differences were observed between males and females. Conclusions: The differences in relative power from eyes-closed to -open conditions are consistent with changes observed in task-based visual sensory responses. Age differences occurred in relatively late developing frontal regions, consistent with canonical attention regions, suggesting that these differences could be reflective of developmental changes in attention processes during puberty. Taken together, resting-state paradigms using eyes-open versus -closed produce distinct results and, in fact, can help pinpoint sensory related brain activity.