The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep
During development, the brain undergoes radical structural and functional changes following a posterior-to-anterior gradient, associated with profound changes of cortical electrical activity during both wakefulness and sleep. However, a systematic assessment of the developmental effects on aperiodic...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-08-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811923004159 |
| _version_ | 1797785524400816128 |
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| author | Jacopo Favaro Michele Angelo Colombo Ezequiel Mikulan Stefano Sartori Margherita Nosadini Maria Federica Pelizza Mario Rosanova Simone Sarasso Marcello Massimini Irene Toldo |
| author_facet | Jacopo Favaro Michele Angelo Colombo Ezequiel Mikulan Stefano Sartori Margherita Nosadini Maria Federica Pelizza Mario Rosanova Simone Sarasso Marcello Massimini Irene Toldo |
| author_sort | Jacopo Favaro |
| collection | DOAJ |
| description | During development, the brain undergoes radical structural and functional changes following a posterior-to-anterior gradient, associated with profound changes of cortical electrical activity during both wakefulness and sleep. However, a systematic assessment of the developmental effects on aperiodic EEG activity maturation across vigilance states is lacking, particularly regarding its topographical aspects. Here, in a population of 160 healthy infants, children and teenagers (from 2 to 17 years, 10 subjects for each year), we investigated the development of aperiodic EEG activity in wakefulness and sleep. Specifically, we parameterized the shape of the aperiodic background of the EEG Power Spectral Density (PSD) by means of the spectral exponent and offset; the exponent reflects the rate of exponential decay of power over increasing frequencies and the offset reflects an estimate of the y-intercept of the PSD.We found that sleep and development caused the EEG-PSD to rotate over opposite directions: during wakefulness the PSD showed a flatter decay and reduced offset over development, while during sleep it showed a steeper decay and a higher offset as sleep becomes deeper. During deep sleep (N2, N3) only the spectral offset decreased over age, indexing a broad-band voltage reduction. As a result, the difference between values in deep sleep and those in both light sleep (N1) and wakefulness increased with age, suggesting a progressive differentiation of wakefulness from sleep EEG activity, most prominent over the frontal regions, the latest to complete maturation. Notably, the broad-band spectral exponent values during deep sleep stages were entirely separated from wakefulness values, consistently across developmental ages and in line with previous findings in adults. Concerning topographical development, the location showing the steepest PSD decay and largest offset shifted from posterior to anterior regions with age. This shift, particularly evident during deep sleep, paralleled the migration of sleep slow wave activity and was consistent with neuroanatomical and cognitive development.Overall, aperiodic EEG activity distinguishes wakefulness from sleep regardless of age; while, during development, it reveals a postero-anterior topographical maturation and a progressive differentiation of wakefulness from sleep. Our study could help to interpret changes due to pathological conditions and may elucidate the neurophysiological processes underlying the development of wakefulness and sleep. |
| first_indexed | 2024-03-13T00:55:18Z |
| format | Article |
| id | doaj.art-8a730c2d8a564e948630983e1bb33e71 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-03-13T00:55:18Z |
| publishDate | 2023-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-8a730c2d8a564e948630983e1bb33e712023-07-07T04:26:39ZengElsevierNeuroImage1095-95722023-08-01277120264The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleepJacopo Favaro0Michele Angelo Colombo1Ezequiel Mikulan2Stefano Sartori3Margherita Nosadini4Maria Federica Pelizza5Mario Rosanova6Simone Sarasso7Marcello Massimini8Irene Toldo9Pediatric Neurology and Neurophysiology Unit, Department of Women's and Children Health, University of Padua, 35128, Padua, Italy; Corresponding authors.Department of Clinical and Biomedical Sciences, University of Milan, 20157, Milan, Italy; Corresponding authors.Department of Clinical and Biomedical Sciences, University of Milan, 20157, Milan, ItalyPediatric Neurology and Neurophysiology Unit, Department of Women's and Children Health, University of Padua, 35128, Padua, Italy; Neuroimmunology Group, Pediatric Research Institute “Città della Speranza”, 35127, Padua, Italy; Department of Neuroscience, University of Padua, 35121, Padua, ItalyPediatric Neurology and Neurophysiology Unit, Department of Women's and Children Health, University of Padua, 35128, Padua, Italy; Neuroimmunology Group, Pediatric Research Institute “Città della Speranza”, 35127, Padua, ItalyPediatric Neurology and Neurophysiology Unit, Department of Women's and Children Health, University of Padua, 35128, Padua, ItalyDepartment of Clinical and Biomedical Sciences, University of Milan, 20157, Milan, ItalyDepartment of Clinical and Biomedical Sciences, University of Milan, 20157, Milan, ItalyDepartment of Clinical and Biomedical Sciences, University of Milan, 20157, Milan, Italy; IRCCS, Fondazione Don Carlo Gnocchi Onlus, 20148, Milan, Italy; Corresponding authors.Pediatric Neurology and Neurophysiology Unit, Department of Women's and Children Health, University of Padua, 35128, Padua, ItalyDuring development, the brain undergoes radical structural and functional changes following a posterior-to-anterior gradient, associated with profound changes of cortical electrical activity during both wakefulness and sleep. However, a systematic assessment of the developmental effects on aperiodic EEG activity maturation across vigilance states is lacking, particularly regarding its topographical aspects. Here, in a population of 160 healthy infants, children and teenagers (from 2 to 17 years, 10 subjects for each year), we investigated the development of aperiodic EEG activity in wakefulness and sleep. Specifically, we parameterized the shape of the aperiodic background of the EEG Power Spectral Density (PSD) by means of the spectral exponent and offset; the exponent reflects the rate of exponential decay of power over increasing frequencies and the offset reflects an estimate of the y-intercept of the PSD.We found that sleep and development caused the EEG-PSD to rotate over opposite directions: during wakefulness the PSD showed a flatter decay and reduced offset over development, while during sleep it showed a steeper decay and a higher offset as sleep becomes deeper. During deep sleep (N2, N3) only the spectral offset decreased over age, indexing a broad-band voltage reduction. As a result, the difference between values in deep sleep and those in both light sleep (N1) and wakefulness increased with age, suggesting a progressive differentiation of wakefulness from sleep EEG activity, most prominent over the frontal regions, the latest to complete maturation. Notably, the broad-band spectral exponent values during deep sleep stages were entirely separated from wakefulness values, consistently across developmental ages and in line with previous findings in adults. Concerning topographical development, the location showing the steepest PSD decay and largest offset shifted from posterior to anterior regions with age. This shift, particularly evident during deep sleep, paralleled the migration of sleep slow wave activity and was consistent with neuroanatomical and cognitive development.Overall, aperiodic EEG activity distinguishes wakefulness from sleep regardless of age; while, during development, it reveals a postero-anterior topographical maturation and a progressive differentiation of wakefulness from sleep. Our study could help to interpret changes due to pathological conditions and may elucidate the neurophysiological processes underlying the development of wakefulness and sleep.http://www.sciencedirect.com/science/article/pii/S1053811923004159Functional brain development1/f noiseEEGAperiodic activitySleep |
| spellingShingle | Jacopo Favaro Michele Angelo Colombo Ezequiel Mikulan Stefano Sartori Margherita Nosadini Maria Federica Pelizza Mario Rosanova Simone Sarasso Marcello Massimini Irene Toldo The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep NeuroImage Functional brain development 1/f noise EEG Aperiodic activity Sleep |
| title | The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep |
| title_full | The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep |
| title_fullStr | The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep |
| title_full_unstemmed | The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep |
| title_short | The maturation of aperiodic EEG activity across development reveals a progressive differentiation of wakefulness from sleep |
| title_sort | maturation of aperiodic eeg activity across development reveals a progressive differentiation of wakefulness from sleep |
| topic | Functional brain development 1/f noise EEG Aperiodic activity Sleep |
| url | http://www.sciencedirect.com/science/article/pii/S1053811923004159 |
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