Abstract
Structural brain connections develop atypically in very preterm children, and altered functional connectivity is also evident in fMRI studies. Such alterations in brain network connectivity are associated with cognitive difficulties in this population. Little is known, however, about electrophysiological interactions among specific brain networks in children born very preterm. In the present study, we recorded magnetoencephalography while very preterm children and full-term controls performed a visual short-term memory task. Regions expressing task-dependent activity changes were identified using beamformer analysis, and inter-regional phase synchrony was calculated. Very preterm children expressed altered regional recruitment in distributed networks of brain areas, across standard physiological frequency ranges including the theta, alpha, beta and gamma bands. Reduced oscillatory synchrony was observed among task-activated brain regions in very preterm children, particularly for connections involving areas critical for executive abilities, including middle frontal gyrus. These findings suggest that inability to recruit neurophysiological activity and interactions in distributed networks including frontal regions may contribute to difficulties in cognitive development in children born very preterm.
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References
Allen MC (2008) Neurodevelopmental outcomes of preterm infants. Curr Opin Neurobiol 21:123–128
Anderson PJ, Doyle LW (2004) Executive functioning in school-age children who were born very preterm of with extremely low birth weight in the 1990s. Pediatrics 114(1):50–57
Back SA, Miller SP (2014) Brain injury in premature neonates: a primary cerebral dysmaturation disorder? Ann Neurol 75(4):470–486
Back SA, Han BH, Luo NL, Chricton CA et al (2002) Selective vulnerability oflate oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 15(22):455–463
Back SA, Riddle A, McClure MM (2007) Maturation-dependent vulnerability ofperinatal white matter in premature birth. Stroke 38(2):724–730
Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc Series B (Methodological) 57(1):289–300
Brookes M, Vrba J, Robinson S, Stevenson C, Peters A, Barnes G, Hillebrand A, Morris P (2008) Optimising experimental design for MEG beamformer imaging. Neuroimage 39:1788–1802
Brookes M, Zumer J, Stevenson C, Hale J, Barnes G, Vrba J, Morris P (2010) Investigating spatial specificity and data averaging in MEG. NeuroImage 49:525–538
Brummelte S, Grunau RE, Chau V, Poskitt KJ, Brant R, Vinall J, Gover A, Synnes AR, Miller SP (2012) Procedural pain and brain development in premature newborns. Ann Neurol 71(3):385–396
Busch NA, Herrmann CS (2003) Object-load and feature-load modulate EEG in a short-term memory task. NeuroReport 14(13):1721–1724
Cunnigham FG, Levenko KJ, Bloom SL, Hauth JC, Rouse DJ, Spong CY (2009) Williams Obstetrics, 23d edn. McGraw-Hill Professional, New York
Doesburg SM, Herdman AT, Ribary U, Cheung T et al (2010) Long-range synchronization and local desynchronization of alpha oscillations during visual short-term memory retention in children. Exp Brain Res 201(4):719–727
Doesburg SM, Ribary U, Herdman AT, Miller SP, Poskitt KJ, Moiseev A, Whitfield MF, Synnes A, Grunau RE (2011a) Altered long-range alpha-band synchronization during visual short-term memory retention in children born very preterm. Neuroimage 54(3):2330–2339
Doesburg SM, Ribary U, Herdman AT, Moiseev A, Cheung T, Miller SP, Poskitt KJ, Weinberg H, Whitfield MF, Synnes A, Grunau RE (2011b) Magnetoencephalography reveals slowing of resting peak oscillatory frequency in children born very preterm. Pediatr Res 70(2):171–175
Doesburg SM, Chau C, Cheung T, Moiseev A, Ribary U, Herdman AT, Miller SP, Cepeda IL, Synnes A, Grunau RE (2013) Neonatal pain, development of functional cortical activity and school-age cognitive outcome in children born at extremely low gestational age. Pain 154:1946–1952
Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224
Frye RE, Malmberg B, Desouza L, Swank P, Smith K, Landry S (2009) Increased prefrontal activation in adolescents born prematurely at high risk during a reading task. Brain Res 1303:111–119
Frye RE, Malmberg B, McLean J III, Swank P et al (2010) Increased left prefrontal activation during an auditory language task in adolescents born preterm at high risk. Brain Res 1336:89–97
Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:1047–3211
Gomarus HK, Althaus M, Wijers AA, Minderaa RB (2006) The effects of memory load and stimulus relevance on the EEG during a visual selective memory search task: an ERP and ERD/ERS study. Clin Neurophysiol 117:871–884
Gregoriou GG, Gotts SJ, Zhou H, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324(5931):1207–1210
Grunau RE, Whitfield MF, Davis C (2002) Pattern of learning disabilities in children with extremely low birth weight and broadly average intelligence. Arch Pediatr Adolesc Med 156(6):615–620
Grunau RE, Haley DW, Whitfield MF, Weinberg J, Yu W, Thiessen P (2007) Altered basal cortisol levels at 3, 6, 8 and 18 months in infants born at extremely low gestational age. J Pediatr 150(2):151–156
Grunau RE, Whitfield MF, Petrie-Thomas J, Synnes AR, Cepeda IL et al (2009) Neonatal pain, parenting stress and interaction, in relation to cognitive and motor development at 8 and 18 months in preterm infants. Pain 143(1–2):138–146
Hari R, Salmelin R (1997) Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci 20(1):44–49
Hart AR, Whitby EW, Griffiths PD, Smith MF (2008) Magnetic resonance imaging and developmental outcome following preterm birth: review of current evidence. Dev Med Child Neurol 50:655–663
Hui HB, Pantazis D, Bressler SL, Leahy RM (2010) Identifying true cortical interactions in MEG using the nulling beamformer. NeuroImage 49:3161–3174
Jensen O, Gelfand J, Kounios J, Lisman JE (2002) Oscillations in the alpha band (9–12 Hz) increase with memory load during retention in a short-term memory task. Cereb Cortex 12:877–882
Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30(7):317–324
Jokisch D, Jensen O (2007) Modulation of gamma and alpha octivity during a working memory task engaging the dorsal or ventral stream. J Neurosci 27:3244–3251
Kaiser J, Lutzenberger W (2005) Human gamma-band activity: a window to cognitive processing. NeuroReport 16(3):0959–4965
Kalpakidou AK, Allin MP, Walshe M, Giampietro V, Kie-woo N, McGuire P, Rifkin L, Murray RM, Nostari C (2012) Neonatal brain injury and neuroanatomy of memory processing following very preterm birth in adulthood: an fMRI study. PLoS ONE 7(4):793–804
Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194–208
Marlow N, Hennessy EM, Bracewell MA, Wolke D (2007) Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics 120:793–804
Mazaheri A, Coffey-Corina S, Mangun GR, Bekker EM (2010) Functional disconnection of frontal cortex and visual cortex in attention-deficit/hyperactivity disorder. Biol Psychiatry 67(7):617–623
McQuillen PS, Ferriero DM (2004) Selective vulnerability in the developing central nervous system. Pediatr Neurol 30:227–235
Ment LR, Hirtz D, Hüppi PS (2009) Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol 8(11):1042–1055
Miller SP, Ferriero DM (2009) From selective vulnerability to connectivity: insights from newborn brain imaging. Trends Neurosci 32(9):496–505
Miskovic V, Schmidt LA, Boyle M, Saigal S (2009) Regional electroencephalogram (EEG) spectral power and hemispheric coherence in young adults born at extremely low birth weight. Clin Neurophysiol 120:231–238
Moiseev A, Gaspar J, Schneider J, Herdman A (2011) Application of multi-source minimum variance beamformers for reconstruction of correlated neural activity. NeuroImage 58:481–496
Mulder H, Pichford NJ, Haggar MS, Marlow N (2009) Development of executive function and attention in preterm children: a systematic review. Dev Neuropsych 34(4):393–421
Murias M, Webb SJ, Greenson J, Dawson G (2007) Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biol Psychiatry 62(3):270–273
Myers EH, Hampson M, Vohr B, Lacadie C, Frost SJ, Pugh KR, Katz KH, Schneider KC, Makuch RW, Constable RT, Ment LR (2010) Functional connectivity to a right hemisphere language center in prematurely born adolescents. Neuroimage 51(4):1445–1452
Nevalainen P, Pihko E, Metsäranta M, Andersson S, Autti T, Lauronen L (2008) Does very premature birth affect the functioning of the somatosensory cortex?–A magnetoencephalography study. Int J Psychophysiol 68(2):85–93
Okumura A, Kubota T, Tsuji T, Kato T, Hayakawa F, Watanabe K (2006) Amplitude spectral analysis of theta/alpha/beta waves in preterm infants. Pediatr Neurol 34:30–34
Palva S, Palva JM (2012) Discovering oscillatory interaction networks with M/EEG: challenges and breakthroughs. Trends Cogn Sci 16(4):219–230
Palva JM, Palva S, Kaila K (2005) Phase synchrony among neuronal oscillations in the human cortex. J Neurosci 25(15):3962–3972
Palva JM, Monto S, Kulashekhar S, Palva S (2010a) Neuronal synchrony reveals working memory networks and predicts individual memory capacity. Proc Natl Acad Sci USA 107(16):7580–7585
Palva S, Monto S, Palva JM (2010b) Graph properties of synchronized cortical networks during visual working memory maintenance. NeuroImage 49(4):3257–3268
Pang EW (2011) Practical aspects of running developmental studies in the MEG. Brain Topogr 24:253–260
Ribary U (2005) Dynamics of thalamo-cortical network oscillations and human perception. Progr Brain Res 150:127–142
Ribary U, Doesburg SM, and Ward LM (2014) Thalamocortical network dynamics: a framework for typical/atypical cortical oscillations and connectivity. In: S.Supek and CJ. Aine (eds) Magnetoencephalography—from signals to dynamic cortical networks, Springer, Verlag Heidelberg, in press
Rickards AL, Kelly EA, Doyle LW, Callanan C (2001) Cognition, academic progress, behavior and self-concept at 14 years of very low birth weight children. J Dev Behav Pediatr 22(1):11–18
Roberts G, Anderson PJ, De Luca C, Doyle LW (2010) Changes in neurodevelopmental outcome at age eight in geographic cohorts of children born at 22–27 weeks gestational age during the 1990s. Arch Dis Child Fetal Neonatal Ed 95(2):90–94
Robinson S, Vrba J (1999) Functional neuroimaging by synthetic aperture magnetometry (SAM), recent advances in biomagnetism. Tohoku University Press, Sendai, pp 302–305
Sarnthein J, Petsche H, Rappelsberger P et al (1998) Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci USA 95:7092–7096
Schack B, Klimesch W (2002) Frequency characteristics of evoked and oscillatory electroencephalic activity in a human memory scanning task. Neurosci Lett 331:107–110
Schafer RJ, Lacadie C, Vohr B, Kesler SR, Katz KH, Schneider KC, Pugh KR, Makuch RW, Reiss AL, Constable RT, Ment LR (2009) Alterations in functional connectivity for language in prematurely born adolescents. Brain 132(Pt 3):661–670
Schlösser RGM, Wagner G, Sauer H (2006) Assessing the working memory network: studies with functional magnetic resonance imaging and structural equation modeling. Neuroscience 139:91–103
Schoffelen J, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30(6):1857–1865
Sekihara K, Nagarajan SS (2008) Adaptive spatial filters for electromagnetic brain imaging. Springer, Berlin
Sekihara K, Nagarajan S, Poeppel D, Marantz A (2002) Performance of an MEG adaptive-beamformer technique in the presence of correlated neural activities: effects on signal intensity and time-course estimates. IEEE Trans Biomed Eng 49(12):1534–1546
Sekihara K, Nagarajan S, Poeppel D, Marantz A (2004) Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction. IEEE Trans Biomed Eng 51(10):1726–1734
Shafer JP (1995) Multiple hypothesis testing. Ann Rev Psychol 46:561–584
Singh KD, Barnes GR, Hillebrand A, Forde EME, Williams AL (2002) Task-related changes in cortical synchronization are spatially coincident with the hemodynamic response. Neuroimage 16:103–114
Smith GC, Gutovich J, Smyser C, Pineda R, Newnham C, Tjoeng TH, Vavasseur C, Wallendorf M, Neil J, Inder T (2011) Neonatal intensive care unit stress is associated with brain development in preterm infants. Ann Neurol 70(4):541–549
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(12):2852–2862
Stipacek A, Grabner RH, Neuper A (2003) Sensitivity of human EEG alpha band desynchronization to different working memory components and increasing levels of memory load. Neurosci Lett 353:193–196
Synnes AR, Anson S, Arkesteijn A, Butt A, Shelagh S, Grunau RE, Rogers M, Whitfield MF (2010) School Entry Age Outcomes for ≤ 800 Gram Birth Weight Babies. J Pediatr 157(6):989–994
Tallon-Baudry C, Bertrand O, Fischer C (2001) Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. J Neurosci 21(RC177):1–5
Taylor HG, Minich NM, Klein N, Hack M (2004) Longitudinal outcomes of very low birth weight: neuropsychological findings. J Int Neuropsychol Soc 10(2):149–163
Thut G, Nietzel A, Brandt SA, Pascual-Leone A (2006) α-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J Neurosci 26:1–5
Uhlhaas PJ, Pipa G, Lima B, Melloni L, Neuenschwander S et al (2009a) Neural synchrony in cortical networks: history, concept and currentstatus. Front Int Neurosci 3(17):1–19
Uhlhaas PJ, Roux F, Singer W, Heanshel C et al (2009b) The development of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proc Natl Acad Sci USA 106(24):9866–9871
Vinall J, Grunau RE (2014) Impact of repeated procedural pain-related stress in infants born very preterm. Pediatr Res 75:584–587. doi:10.1038/pr.2014.16
Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz C (2011) An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. NeuroImage 55:1548–1565
Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8(1):110–124
Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29(4):423–440
Wilson H, Moiseev A, Podin S, Quraan M (2007) Continuous head localization and data correction in MEG. Int Congr Ser 1300:623–626
Worden MS, Foxe JJ, Wang N, Simpson GV (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific a-band electroencephalography increases over occipital cortex. J Neurosci 20(RC63):1–6
Acknowledgments
We would like to thank Dr. Ken Poskitt, pediatric neuroradiologist, for his invaluable role in obtaining the MRI scans. We would like to thank Dr. Ivan Cepeda and Gisela Gosse for coordinating the study, Katia Jitlina, Amanda Degenhardt, Dr. Teresa Cheung, Cecil Chau and Julie Unterman for their help in data collection. This work was supported by Grant RO1 HD039783 from the Eunice Kennedy Shriver Institute of Child Health and Human Development of the National Institutes of Health to R.E.G., the Canadian Institutes of Health Research Grant MOP 86489 to R.E.G., a Senior Scientist Award from the Child and Family Research Institute to R.E.G, support from the BC Leading Edge Endowment Fund (BC LEEF) to U.R., a Canada Foundation for Innovation (CFI) Grant to U.R., the Behavioral and Cognitive Neuroscience Institute (BCNI) to U.R., and Down Syndrome Research Foundation (DSRF: Burnaby, BC, Canada).
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Moiseev, A., Doesburg, S.M., Herdman, A.T. et al. Altered Network Oscillations and Functional Connectivity Dynamics in Children Born Very Preterm. Brain Topogr 28, 726–745 (2015). https://doi.org/10.1007/s10548-014-0416-0
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DOI: https://doi.org/10.1007/s10548-014-0416-0