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

Nathan M Petro; Lauren R Ott; Samantha H Penhale; Maggie P Rempe; Christine M Embury; Giorgia Picci; Yu-Ping Wang; Julia M Stephen; Vince D Calhoun; Tony W Wilson

doi:10.1016/j.neuroimage.2022.119337

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

Neuroimage. 2022 Sep:258:119337. doi: 10.1016/j.neuroimage.2022.119337. Epub 2022 May 27.

Authors

Affiliations

¹ Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USA.
² Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USA; College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA.
³ Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USA; Department of Psychology, University of Nebraska Omaha, Omaha, NE, USA.
⁴ Department of Biomedical Engineering, Tulane University, New Orleans, LA, USA.
⁵ Mind Research Network, Albuquerque, NM, USA.
⁶ Mind Research Network, Albuquerque, NM, USA; Tri-Institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, and Emory University, Atlanta, GA, USA.
⁷ Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USA; Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USA. Electronic address: tony.wilson@boystown.org.

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.

Keywords: Adolescence; Alpha; Beta; MEG; Magnetoencephalography; Oscillations; Resting state.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural

MeSH terms

Adolescent
Attention / physiology
Brain / physiology
Brain Mapping
Child
Electroencephalography* / methods
Eye
Female
Humans
Magnetoencephalography
Male
Occipital Lobe
Rest* / physiology

Abstract

Publication types

MeSH terms

Grants and funding