Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury
Early neurodevelopment is critically dependent on the structure and dynamics of spontaneous neuronal activity; however, the natural organization of newborn cortical networks is poorly understood. Recent adult studies suggest that spontaneous cortical activity exhibits discrete network states with ph...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811923004937 |
| _version_ | 1827853234229739520 |
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| author | Mohammad Khazaei Khadijeh Raeisi Sampsa Vanhatalo Filippo Zappasodi Silvia Comani Anton Tokariev |
| author_facet | Mohammad Khazaei Khadijeh Raeisi Sampsa Vanhatalo Filippo Zappasodi Silvia Comani Anton Tokariev |
| author_sort | Mohammad Khazaei |
| collection | DOAJ |
| description | Early neurodevelopment is critically dependent on the structure and dynamics of spontaneous neuronal activity; however, the natural organization of newborn cortical networks is poorly understood. Recent adult studies suggest that spontaneous cortical activity exhibits discrete network states with physiological correlates. Here, we studied newborn cortical activity during sleep using hidden Markov modeling to determine the presence of such discrete neonatal cortical states (NCS) in 107 newborn infants, with 47 of them presenting with a perinatal brain injury. Our results show that neonatal cortical activity organizes into four discrete NCSs that are present in both cardinal sleep states of a newborn infant, active and quiet sleep, respectively. These NCSs exhibit state-specific spectral and functional network characteristics. The sleep states exhibit different NCS dynamics, with quiet sleep presenting higher fronto-temporal activity and a stronger brain-wide neuronal coupling. Brain injury was associated with prolonged lifetimes of the transient NCSs, suggesting lowered dynamics, or flexibility, in the cortical networks. Taken together, the findings suggest that spontaneously occurring transient network states are already present at birth, with significant physiological and pathological correlates; this NCS analysis framework can be fully automatized, and it holds promise for offering an objective, global level measure of early brain function for benchmarking neurodevelopmental or clinical research. |
| first_indexed | 2024-03-12T11:02:18Z |
| format | Article |
| id | doaj.art-3ccd5d1104e64db4ad24eb79ece798b7 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-03-12T11:02:18Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-3ccd5d1104e64db4ad24eb79ece798b72023-09-02T04:31:20ZengElsevierNeuroImage1095-95722023-10-01279120342Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injuryMohammad Khazaei0Khadijeh Raeisi1Sampsa Vanhatalo2Filippo Zappasodi3Silvia Comani4Anton Tokariev5Department of Neurosciences, Imaging and Clinical Sciences, University “Gabriele d'Annunzio” of Chieti–Pescara, ITAB building, 3rd floor, room 314, Chieti, Via dei Vestini, Italy; Corresponding author.Department of Neurosciences, Imaging and Clinical Sciences, University “Gabriele d'Annunzio” of Chieti–Pescara, ITAB building, 3rd floor, room 314, Chieti, Via dei Vestini, ItalyBABA center, Pediatric Research Center, Departments of Clinical Neurophysiology and Physiology, Children's Hospital, Helsinki University Hospital and University of Helsinki, Helsinki, FinlandDepartment of Neurosciences, Imaging and Clinical Sciences, University “Gabriele d'Annunzio” of Chieti–Pescara, ITAB building, 3rd floor, room 314, Chieti, Via dei Vestini, Italy; Institute for Advanced Biomedical Technologies, University “Gabriele d'Annunzio” of Chieti–Pescara, Chieti, ItalyDepartment of Neurosciences, Imaging and Clinical Sciences, University “Gabriele d'Annunzio” of Chieti–Pescara, ITAB building, 3rd floor, room 314, Chieti, Via dei Vestini, Italy; Behavioral Imaging and Neural Dynamics Center, University “Gabriele d'Annunzio” of Chieti–Pescara, Chieti, ItalyBABA center, Pediatric Research Center, Departments of Clinical Neurophysiology and Physiology, Children's Hospital, Helsinki University Hospital and University of Helsinki, Helsinki, FinlandEarly neurodevelopment is critically dependent on the structure and dynamics of spontaneous neuronal activity; however, the natural organization of newborn cortical networks is poorly understood. Recent adult studies suggest that spontaneous cortical activity exhibits discrete network states with physiological correlates. Here, we studied newborn cortical activity during sleep using hidden Markov modeling to determine the presence of such discrete neonatal cortical states (NCS) in 107 newborn infants, with 47 of them presenting with a perinatal brain injury. Our results show that neonatal cortical activity organizes into four discrete NCSs that are present in both cardinal sleep states of a newborn infant, active and quiet sleep, respectively. These NCSs exhibit state-specific spectral and functional network characteristics. The sleep states exhibit different NCS dynamics, with quiet sleep presenting higher fronto-temporal activity and a stronger brain-wide neuronal coupling. Brain injury was associated with prolonged lifetimes of the transient NCSs, suggesting lowered dynamics, or flexibility, in the cortical networks. Taken together, the findings suggest that spontaneously occurring transient network states are already present at birth, with significant physiological and pathological correlates; this NCS analysis framework can be fully automatized, and it holds promise for offering an objective, global level measure of early brain function for benchmarking neurodevelopmental or clinical research.http://www.sciencedirect.com/science/article/pii/S1053811923004937Neonatal EEGSleepBrain dynamicsFunctional networksHypoxic-ischemic encephalopathy |
| spellingShingle | Mohammad Khazaei Khadijeh Raeisi Sampsa Vanhatalo Filippo Zappasodi Silvia Comani Anton Tokariev Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury NeuroImage Neonatal EEG Sleep Brain dynamics Functional networks Hypoxic-ischemic encephalopathy |
| title | Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| title_full | Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| title_fullStr | Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| title_full_unstemmed | Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| title_short | Neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| title_sort | neonatal cortical activity organizes into transient network states that are affected by vigilance states and brain injury |
| topic | Neonatal EEG Sleep Brain dynamics Functional networks Hypoxic-ischemic encephalopathy |
| url | http://www.sciencedirect.com/science/article/pii/S1053811923004937 |
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