Sleep State-dependent Development of Resting-state Functional Connectivity During the Preterm Period

Overview

Journal Sleep

Publisher Oxford University Press

Specialty Psychiatry

Date 2024 Sep 25

PMID 39320057

Authors

Anna Shiraki

Hiroyuki Kidokoro

Hama Watanabe

Gentaro Taga

Takafumi Ushida

Hajime Narita

Takamasa Mitsumatsu

Sumire Kumai

Ryosuke Suzui

Fumi Sawamura

Yuji Ito

Hiroyuki Yamamoto

Tomohiko Nakata

Yoshiaki Sato

Masahiro Hayakawa

Yoshiyuki Takahashi

Jun Natsume

Affiliations

Soon will be listed here.

Abstract

Study Objectives: The brains of preterm infants exhibit altered functional connectivity (FC) networks, but the potential variation in sleep states and the impact of breathing patterns on FC networks are unclear. This study explores the evolution of resting-state FC from preterm to term, focusing on breathing patterns and distinguishing between active sleep (AS) and quiet sleep (QS).

Methods: We recruited 63 preterm infants and 44 healthy-term infants and performed simultaneous electroencephalography and functional near-infrared spectroscopy. FC was calculated using oxy- and deoxyhemoglobin signals across eight channels. First, FC was compared between periodic breathing (PB) and non-PB segments. Then sleep state-dependent FC development was explored. FC was compared between AS and QS segments and between preterm infants at term and term-born infants in each sleep state. Finally, associations between FC at term, clinical characteristics, and neurodevelopmental outcomes in late infancy were assessed in preterm infants.

Results: In total, 148 records from preterm infants and 44 from term-born infants were analyzed. PB inflated FC values. After excluding PB segments, FC was found to be elevated during AS compared to QS, particularly in connections involving occipital regions. Preterm infants had significantly higher FC in both sleep states compared to term-born infants. Furthermore, stronger FC in specific connections during AS at term was associated with unfavorable neurodevelopment in preterm infants.

Conclusions: Sleep states play a critical role in FC development and preterm infants show observable changes in FC.

Citing Articles

Co-developing sleep-wake and sensory foundations for cognition in the human fetus and newborn.

Whitehead K Dev Cogn Neurosci. 2024; 71():101487.

PMID: 39675060 PMC: 11699341. DOI: 10.1016/j.dcn.2024.101487.

References

Tononi G, Cirelli C . Sleep function and synaptic homeostasis. Sleep Med Rev. 2005; 10(1):49-62. DOI: 10.1016/j.smrv.2005.05.002. View

Yrjola P, Myers M, Welch M, Stevenson N, Tokariev A, Vanhatalo S . Facilitating early parent-infant emotional connection improves cortical networks in preterm infants. Sci Transl Med. 2022; 14(664):eabq4786. DOI: 10.1126/scitranslmed.abq4786. View

Spoormaker V, Schroter M, Gleiser P, Andrade K, Dresler M, Wehrle R . Development of a large-scale functional brain network during human non-rapid eye movement sleep. J Neurosci. 2010; 30(34):11379-87. PMC: 6633325. DOI: 10.1523/JNEUROSCI.2015-10.2010. View

Dereymaeker A, Pillay K, Vervisch J, De Vos M, Van Huffel S, Jansen K . Review of sleep-EEG in preterm and term neonates. Early Hum Dev. 2017; 113:87-103. PMC: 6342258. DOI: 10.1016/j.earlhumdev.2017.07.003. View

Uchitel J, Vanhatalo S, Austin T . Early development of sleep and brain functional connectivity in term-born and preterm infants. Pediatr Res. 2021; 91(4):771-786. DOI: 10.1038/s41390-021-01497-4. View

Damaraju E, Tagliazucchi E, Laufs H, Calhoun V . Connectivity dynamics from wakefulness to sleep. Neuroimage. 2020; 220:117047. PMC: 7753906. DOI: 10.1016/j.neuroimage.2020.117047. View

Urlesberger B, Pichler G, Gradnitzer E, Reiterer F, Zobel G, Muller W . Changes in cerebral blood volume and cerebral oxygenation during periodic breathing in term infants. Neuropediatrics. 2000; 31(2):75-81. DOI: 10.1055/s-2000-7477. View

Gao W, Alcauter S, Smith J, Gilmore J, Lin W . Development of human brain cortical network architecture during infancy. Brain Struct Funct. 2014; 220(2):1173-86. PMC: 4850360. DOI: 10.1007/s00429-014-0710-3. View

Sasai S, Homae F, Watanabe H, Sasaki A, Tanabe H, Sadato N . A NIRS-fMRI study of resting state network. Neuroimage. 2012; 63(1):179-93. DOI: 10.1016/j.neuroimage.2012.06.011. View

10.

Hong C, Harris J, Pearlson G, Kim J, Calhoun V, Fallon J . fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Hum Brain Mapp. 2008; 30(5):1705-22. PMC: 2753360. DOI: 10.1002/hbm.20635. View

11.

Tokariev A, Roberts J, Zalesky A, Zhao X, Vanhatalo S, Breakspear M . Large-scale brain modes reorganize between infant sleep states and carry prognostic information for preterms. Nat Commun. 2019; 10(1):2619. PMC: 6565810. DOI: 10.1038/s41467-019-10467-8. View

12.

Wang Z, Fei X, Liu X, Wang Y, Hu Y, Peng W . REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex. Nat Commun. 2022; 13(1):6896. PMC: 9653484. DOI: 10.1038/s41467-022-34720-9. View

13.

Patel M, Mohr M, Lake D, Delos J, Moorman J, Sinkin R . Clinical associations with immature breathing in preterm infants: part 2-periodic breathing. Pediatr Res. 2016; 80(1):28-34. PMC: 4929034. DOI: 10.1038/pr.2016.58. View

14.

De Asis-Cruz J, Kapse K, Basu S, Said M, Scheinost D, Murnick J . Functional brain connectivity in ex utero premature infants compared to in utero fetuses. Neuroimage. 2020; 219:117043. PMC: 7493786. DOI: 10.1016/j.neuroimage.2020.117043. View

15.

DallOrso S, Arichi T, Fitzgibbon S, Edwards A, Burdet E, Muceli S . Development of functional organization within the sensorimotor network across the perinatal period. Hum Brain Mapp. 2022; 43(7):2249-2261. PMC: 8996360. DOI: 10.1002/hbm.25785. View

16.

Del Rio-Bermudez C, Blumberg M . Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks. Bioessays. 2018; 40(4):e1700234. PMC: 6247910. DOI: 10.1002/bies.201700234. View

17.

Inder T, Volpe J, Anderson P . Defining the Neurologic Consequences of Preterm Birth. N Engl J Med. 2023; 389(5):441-453. DOI: 10.1056/NEJMra2303347. View

18.

Arimitsu T, Shinohara N, Minagawa Y, Hoshino E, Hata M, Takahashi T . Differential age-dependent development of inter-area brain connectivity in term and preterm neonates. Pediatr Res. 2022; 92(4):1017-1025. PMC: 9586860. DOI: 10.1038/s41390-022-01939-7. View

19.

Lynch C, Silver B, Dubin M, Martin A, Voss H, Jones R . Prevalent and sex-biased breathing patterns modify functional connectivity MRI in young adults. Nat Commun. 2020; 11(1):5290. PMC: 7576607. DOI: 10.1038/s41467-020-18974-9. View

20.

Andre M, Lamblin M, dAllest A, Curzi-Dascalova L, Moussalli-Salefranque F, S Nguyen The T . Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol Clin. 2010; 40(2):59-124. DOI: 10.1016/j.neucli.2010.02.002. View