Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development
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. S...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-09-01
|
| Series: | NeuroImage |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811922004566 |
| _version_ | 1818114567763394560 |
|---|---|
| author | 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 |
| author_facet | 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 |
| author_sort | Nathan M. Petro |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-11T03:52:47Z |
| format | Article |
| id | doaj.art-0d40c5bc52e544aaacce996cf6b150d7 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-11T03:52:47Z |
| publishDate | 2022-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-0d40c5bc52e544aaacce996cf6b150d72022-12-22T01:21:52ZengElsevierNeuroImage1095-95722022-09-01258119337Eyes-closed versus eyes-open differences in spontaneous neural dynamics during developmentNathan M. Petro0Lauren R. Ott1Samantha H. Penhale2Maggie P. Rempe3Christine M. Embury4Giorgia Picci5Yu-Ping Wang6Julia M. Stephen7Vince D. Calhoun8Tony W. Wilson9Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USABoys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USABoys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USABoys 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, USABoys 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, USABoys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USADepartment of Biomedical Engineering, Tulane University, New Orleans, LA, USAMind Research Network, Albuquerque, NM, USAMind 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, USABoys 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; Corresponding author at: Boys Town National Research Hospital, Institute for Human Neuroscience, 378 Bucher Circle, Boys Town, NE 68010, USA.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.http://www.sciencedirect.com/science/article/pii/S1053811922004566MagnetoencephalographyMEGOscillationsResting stateBetaAlpha |
| spellingShingle | 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 Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development NeuroImage Magnetoencephalography MEG Oscillations Resting state Beta Alpha |
| title | Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development |
| title_full | Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development |
| title_fullStr | Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development |
| title_full_unstemmed | Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development |
| title_short | Eyes-closed versus eyes-open differences in spontaneous neural dynamics during development |
| title_sort | eyes closed versus eyes open differences in spontaneous neural dynamics during development |
| topic | Magnetoencephalography MEG Oscillations Resting state Beta Alpha |
| url | http://www.sciencedirect.com/science/article/pii/S1053811922004566 |
| work_keys_str_mv | AT nathanmpetro eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT laurenrott eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT samanthahpenhale eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT maggieprempe eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT christinemembury eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT giorgiapicci eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT yupingwang eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT juliamstephen eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT vincedcalhoun eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment AT tonywwilson eyesclosedversuseyesopendifferencesinspontaneousneuraldynamicsduringdevelopment |