Abstract
Little is known about the frequency features of spontaneous neural activity in the brains of moderate and late preterm (MLPT) newborns. We used resting-state functional magnetic resonance imaging (rs-fMRI) and the amplitude of low-frequency fluctuation (ALFF) method to investigate the frequency properties of spontaneous blood oxygen level-dependent (BOLD) signals in 26 MLPT and 35 term newborns. Two frequency bands, slow-4 (0.027–0.073 Hz) and slow-5 (0.01–0.027 Hz), were analyzed. Our results showed widespread differences in ALFF between the two bands; differences occurred mainly in the primary sensory and motor cortices and to a lesser extent in association cortices and subcortical areas. Compared with term newborns, MLPT newborns showed significantly altered neural activity predominantly in the primary sensory and motor cortices and in the posterior cingulate gyrus/precuneus. In addition, a significant interaction between frequency bands and groups was observed in the primary somatosensory cortex. Intriguingly, these primary sensory and motor regions have been proven to be the major cortical hubs during the neonatal period. Our results revealed the frequency of spontaneous BOLD signal differences between MLPT and term newborns, which contribute to the understanding of regional development of spontaneous brain rhythms of MLPT newborns.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alcauter S, Lin W, Smith JK, Goldman BD, Reznick JS, Gilmore JH, Gao W (2014) Frequency of spontaneous BOLD signal shifts during infancy and correlates with cognitive performance. Dev Cognit Neurosci 12:40–50. doi:10.1016/j.dcn.2014.10.004
Arnstein D, Cui F, Keysers C, Maurits NM, Gazzola V (2011) mu-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. J Neurosci 31:14243–14249. doi:10.1523/jneurosci.0963-11.2011
Barker DP, Rutter N (1995) Exposure to invasive procedures in neonatal intensive care unit admissions. Arch Dis Child Fet Neonatal Ed 72:F47–F48
Batuev AS, Iovleva NN, Koshchavtsev AG (2008) Comparative analysis of the EEG in babies in the first month of life with gestation periods of 30–42 weeks. Neurosci Behav Physiol 38:621–626. doi:10.1007/s11055-008-9018-1
Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 37:90–101. doi:10.1016/j.neuroimage.2007.04.042
Berchicci M et al (2011) Development of mu rhythm in infants and preschool children. Dev Neurosci 33:130–143. doi:10.1159/000329095
Berchicci M, Tamburro G, Comani S (2015) The intrahemispheric functional properties of the developing sensorimotor cortex are influenced by maturation. Front hum neurosci 9:39. doi:10.3389/fnhum.2015.00039
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541
Blencowe H et al (2012) National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379:2162–2172. doi:10.1016/s0140-6736(12)60820-4
Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929. doi:10.1126/science.1099745
Cao M et al (2016) Early development of functional network segregation revealed by connectomic analysis of the preterm human brain. Cereb cortex. doi:10.1093/cercor/bhw038
Chugani HT (1998) A critical period of brain development: studies of cerebral glucose utilization with PET. Prev Med 27:184–188. doi:10.1006/pmed.1998.0274
Chumbley J, Worsley K, Flandin G, Friston K (2010) Topological FDR for neuroimaging. NeuroImage 49:3057–3064. doi:10.1016/j.neuroimage.2009.10.090
Cusack R, Brett M, Osswald K (2003) An evaluation of the use of magnetic field maps to undistort echo-planar images. NeuroImage 18:127–142
Davidson AJ (2007) Awareness, dreaming and unconscious memory formation during anaesthesia in children. Best Pract Res Clin Anaesthesiol 21:415–429
DeCasper AJ, Fifer WP (1980) Of human bonding: newborns prefer their mothers’ voices. Science 208:1174–1176
Deichmann R, Josephs O, Hutton C, Corfield DR, Turner R (2002) Compensation of susceptibility-induced BOLD sensitivity losses in echo-planar fMRI imaging. NeuroImage 15:120–135. doi:10.1006/nimg.2001.0985
Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Huppi PS, Hertz-Pannier L (2013) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience. doi:10.1016/j.neuroscience.2013.12.044
Engle WA (2004) Age terminology during the perinatal period. Pediatrics 114:1362–1364. doi:10.1542/peds.2004-1915
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711. doi:10.1038/nrn2201
Fransson P, Skiold B, Horsch S, Nordell A, Blennow M, Lagercrantz H, Aden U (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci 104:15531–15536. doi:10.1073/pnas.0704380104
Fransson P, Aden U, Blennow M, Lagercrantz H (2011) The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb cortex 21:145–154. doi:10.1093/cercor/bhq071
Fransson P, Metsaranta M, Blennow M, Aden U, Lagercrantz H, Vanhatalo S (2013) Early development of spatial patterns of power-law frequency scaling in fMRI resting-state and EEG data in the newborn brain. Cereb cortex 23:638–646. doi:10.1093/cercor/bhs047
Gao W, Zhu H, Giovanello KS, Smith JK, Shen D, Gilmore JH, Lin W (2009) Evidence on the emergence of the brain’s default network from 2 week-old to 2 year-old healthy pediatric subjects. Proc Natl Acad Sci 106:6790–6795. doi:10.1073/pnas.0811221106
Gao W, Gilmore JH, Giovanello KS, Smith JK, Shen D, Zhu H, Lin W (2011) Temporal and spatial evolution of brain network topology during the first two years of life. PloS One 6:e25278. doi:10.1371/journal.pone.0025278
Gilmore JH et al (2012) Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cereb Cortex 22:2478–2485. doi:10.1093/cercor/bhr327
Gläscher J, Gitelman D (2008) Contrast weights in flexible factorial design with multiple groups of subjects SPM@ JISCMAIL AC UK Sml, editor
Gohel SR, Biswal BB (2015) Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain connect 5:23–34. doi:10.1089/brain.2013.0210
Han Y et al (2011) Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: a resting-state fMRI study. NeuroImage 55:287–295. doi:10.1016/j.neuroimage.2010.11.059
He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME (2008) Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture. Proc Natl Acad Sci 105:16039–16044. doi:10.1073/pnas.0807010105
Hou Y, Wu X, Hallett M, Chan P, Wu T (2014) Frequency-dependent neural activity in Parkinson’s disease. Hum Brain Mapp 35:5815–5833. doi:10.1002/hbm.22587
Iai M, Yamamura T, Takashima S (1997) Early expression of proteolipid protein in human fetal and infantile cerebri. Pediatr Neurol 17:235–239
Karniski W (1992) The late somatosensory evoked potential in premature and term infants. I. Principal component topography. Electroencephalogr Clin Neurophysiol 84:32–43
Karniski W, Wyble L, Lease L, Blair RC (1992) The late somatosensory evoked potential in premature and term infants. II. Topography and latency development. Electroencephalogr Clin Neurophysiol 84:44–54
Kelly CE et al (2015) Moderate and late preterm infants exhibit widespread brain white matter microstructure alterations at term-equivalent age relative to term-born controls. Brain Imaging Behav. doi:10.1007/s11682-015-9361-0
Kinney HC (2006) The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol 30:81–88. doi:10.1053/j.semperi.2006.02.006
Kolata G (1984) Studying learning in the womb. Science 225:302–303
Kostovic I, Jovanov-Milosevic N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fet Neonatal Med 11:415–422. doi:10.1016/j.siny.2006.07.001
Kostovic I, Judas M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99:1119–1127. doi:10.1111/j.1651-2227.2010.01811.x
Lagercrantz H, Changeux JP (2009) The emergence of human consciousness: from fetal to neonatal life. Pediatr Res 65:255–260. doi:10.1203/PDR.0b013e3181973b0d
Lodygensky GA, Vasung L, Sizonenko SV, Huppi PS (2010) Neuroimaging of cortical development and brain connectivity in human newborns and animal models. J Anat 217:418–428. doi:10.1111/j.1469-7580.2010.01280.x
Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci 104:13170–13175. doi:10.1073/pnas.0700668104
McKinstry RC et al (2002) Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb cortex 12:1237–1243
Munakata S et al (2013) Gray matter volumetric MRI differences late-preterm and term infants. Brain Dev 35:10–16. doi:10.1016/j.braindev.2011.12.011
Myers MM, Grieve PG, Izraelit A, Fifer WP, Isler JR, Darnall RA, Stark RI (2012) Developmental profiles of infant EEG: overlap with transient cortical circuits. Clin Neurophysiol 123:1502–1511. doi:10.1016/j.clinph.2011.11.264
Penttonen M, Buzsáki G (2003) Natural logarithmic relationship between brain oscillators. Thal Relat Syst 2:145–152. doi:10.1017/S1472928803000074
Pike AA, Marlow N, Dawson C (1997) Posterior tibial somatosensory evoked potentials in very preterm infants. Early Hum Dev 47:71–84
Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154. doi:10.1016/j.neuroimage.2011.10.018
Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 84:320–341. doi:10.1016/j.neuroimage.2013.08.048
Raju TN (2012) Developmental physiology of late and moderate prematurity. Semin Fet Neonatal Med 17:126–131. doi:10.1016/j.siny.2012.01.010
Sankupellay M, Wilson S, Heussler HS, Parsley C, Yuill M, Dakin C (2011) Characteristics of sleep EEG power spectra in healthy infants in the first two years of life. Clin Neurophysiol 122:236–243. doi:10.1016/j.clinph.2010.06.030
Shi F, Yap PT, Wu G, Jia H, Gilmore JH, Lin W, Shen D (2011) Infant brain atlases from neonates to 1 and 2 year-olds. PLoS One 6:e18746. doi:10.1371/journal.pone.0018746
Smit BJ, Ongerboer de Visser BW, de Vries LS, Dekker FW, Kok JH (2000) Somatosensory evoked potentials in very preterm infants. Clin Neurophysiol 111:901–908
Smyser CD, Neil JJ (2015) Use of resting-state functional MRI to study brain development and injury in neonates. Semin Perinatol 39:130–140. doi:10.1053/j.semperi.2015.01.006
Smyser CD, Inder TE, Shimony JS, Hill JE, Degnan AJ, Snyder AZ, Neil JJ (2010) Longitudinal analysis of neural network development in preterm infants. Cereb cortex 20:2852–2862. doi:10.1093/cercor/bhq035
Song XW et al (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031. doi:10.1371/journal.pone.0025031
Tau GZ, Peterson BS (2010) Normal development of brain circuits. Neuropsychopharmacology 35:147–168. doi:10.1038/npp.2009.115
Tolonen M, Palva JM, Andersson S, Vanhatalo S (2007) Development of the spontaneous activity transients and ongoing cortical activity in human preterm babies. Neuroscience 145:997–1006. doi:10.1016/j.neuroscience.2006.12.070
Vanhatalo S, Kaila K (2006) Development of neonatal EEG activity: from phenomenology to physiology. Semin Fet Neonatal Med 11:471–478. doi:10.1016/j.siny.2006.07.008
Walsh JM, Doyle LW, Anderson PJ, Lee KJ, Cheong JL (2014) Moderate and late preterm birth: effect on brain size and maturation at term-equivalent age. Radiology 273:232–240. doi:10.1148/radiol.14132410
Weber F (2010) Evidence for the need for anaesthesia in the neonate. Best Pract Res Clin Anaesthesiol 24:475–484
Wei L et al (2014) Specific frequency bands of amplitude low-frequency oscillation encodes personality. Hum Brain Mapp 35:331–339. doi:10.1002/hbm.22176
Xu G et al (2011) Late development of the GABAergic system in the human cerebral cortex and white matter. J Neuropathol Exp Neurol 70:841–858. doi:10.1097/NEN.0b013e31822f471c
Yan CG et al (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. NeuroImage 76:183–201. doi:10.1016/j.neuroimage.2013.03.004
Zang YF et al (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29:83–91. doi:10.1016/j.braindev.2006.07.002
Zhang J et al (2013) Specific frequency band of amplitude low-frequency fluctuation predicts Parkinson’s disease. Behav Brain Res 252:18–23. doi:10.1016/j.bbr.2013.05.039
Zuo XN et al (2010) The oscillating brain: complex and reliable. NeuroImage 49:1432–1445. doi:10.1016/j.neuroimage.2009.09.037
Acknowledgments
This study was funded by the National Science Foundation of China (Grant No. 81173662 to Y.S.) and the Programs for the Development of Science and Technology of Chongqing in China (Grant No. 2011GGC083 to Y.S.). We thank all the families who participated in this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest.
Ethical Approval
This study was approved by the Ethics Committee of Daping Hospital, Third Military Medical University (Chongqing, China). All study procedures were in accordance with the Declaration of Helsinki (2008 revision).
Informed Consent
Parental informed, written consent was obtained for each subject prior to participation in the study.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wu, X., Wei, L., Wang, N. et al. Frequency of Spontaneous BOLD Signal Differences between Moderate and Late Preterm Newborns and Term Newborns. Neurotox Res 30, 539–551 (2016). https://doi.org/10.1007/s12640-016-9642-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12640-016-9642-4