The maturation of cortical sleep rhythms and networks over early development

Clinical Neurophysiology

Volumn 125, Issue 7, 2014, Pages 1360-1370

  Chu, C J ^a,b   Leahy, J ^a   Pathmanathan, J ^a,b   Kramer, M A ^c   Cash, S S ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Boston University   (United States)

Author keywords

Brain networks; Brain rhythms; Development; EEG; Functional connectivity; Sleep

Indexed keywords

ADOLESCENCE; ALPHA RHYTHM; ARTICLE; BETA RHYTHM; BIRTH; BRAIN DEVELOPMENT; BRAIN MATURATION; BRAIN REGION; CEPHALOMETRY; CHILD; CHILDHOOD; COHORT ANALYSIS; DENSITY; ELECTRIC POTENTIAL; ELECTRODE; ELECTROENCEPHALOGRAM; FEMALE; HIGH FREQUENCY OSCILLATION; HUMAN; HUMAN EXPERIMENT; INFANT; MALE; MEDICAL RECORD REVIEW; NEWBORN; NORMAL HUMAN; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SKULL; SLEEP PATTERN; TEMPORAL LOBE; ADOLESCENT; ANALYSIS OF VARIANCE; ARTIFICIAL NEURAL NETWORK; BRAIN CORTEX; BRAIN MAPPING; CIRCADIAN RHYTHM; ELECTROENCEPHALOGRAPHY; ELECTROOCULOGRAPHY; GROWTH, DEVELOPMENT AND AGING; NERVE CELL NETWORK; PHYSIOLOGY; PRESCHOOL CHILD; PROCEDURES; REFERENCE VALUE; SLEEP;

ADOLESCENT; ANALYSIS OF VARIANCE; BRAIN MAPPING; CEREBRAL CORTEX; CHILD; CHILD, PRESCHOOL; CIRCADIAN RHYTHM; ELECTROENCEPHALOGRAPHY; ELECTROOCULOGRAPHY; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; MALE; NERVE NET; NEURAL NETWORKS (COMPUTER); REFERENCE VALUES; SLEEP;

EID: 84901285753     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2013.11.028     Document Type: Article

References (84)

1. Anders T.F. The infant sleep profile. Neuropadiatrie 1974, 5:425-442.
2. Andrade-Valenca L.P., Dubeau F., Mari F., Zelmann R., Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 2011, 77:524-531.
3. Baho E., Di Cristo G. Neural activity and neurotransmission regulate the maturation of the innervation field of cortical GABAergic interneurons in an age-dependent manner. J Neurosci 2012, 32:911-918.
4. Baker F.C., Turlington S.R., Colrain I. Developmental changes in the sleep electroencephalogram of adolescent boys and girls. J Sleep Res 2012, 21:59-67.
5. Ball T., Demandt E., Mutschler I., Neitzel E., Mehring C., Vogt K., et al. Movement related activity in the high gamma range of the human EEG. Neuroimage 2008, 41:302-310.
6. Baria A.T., Baliki M.N., Parrish T., Apkarian A.V. Anatomical and functional assemblies of brain BOLD oscillations. J Neurosci 2011, 31:7910-7919.
7. Ben-Ari Y., Woodin M.A., Sernagor E., Cancedda L., Vinay L., Rivera C., et al. Refuting the challenges of the developmental shift of polarity of GABA actions: GABA more exciting than ever!. Front Cell Neurosci 2012, 6:35.
8. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B (Methodological) 1995, 57:289-300.
9. Bollimunta A., Mo J., Schroeder C.E., Ding M. Neuronal mechanisms and attentional modulation of corticothalamic α oscillations. J Neurosci 2011, 31:4935-4943.
10. Bronzino JD, The biomedical engineering handbook, 2nd ed. CRC Press: Boca Raton, NO, 2000.
11. Buzsáki G. Large-scale recording of neuronal ensembles. Nat Neurosci 2004, 7:446-451.
12. Buszaki G. Rhythms of the brain 2006, Oxford University Press, New York.
13. Buzsaki G., Draguhn A. Neuronal oscillations in cortical networks. Science 2004, 304:1926-1929.
14. Buzsaki G., Watson B.O. Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin Neurosci 2012, 14:345-367.
15. Campbell I.G., Feinberg I. Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. PNAS 2009, 106:5177-5180.
16. Canolty R.T., Knight R.T. The functional role of cross-frequency coupling. Trends Cogn Sci 2010, 11:506-515.
17. Chu C.J., Kramer M.A., Pathmanathan J., Bianchi M.T., Westover M.B., Wizon L., et al. Emergence of stable functional networks in long-term human electroencephalography. J Neurosci 2012, 32:2703-2713.
18. Darvas F., Scherer R., Ojemann J.G., Rao R.P., Miller K.J., Sorensen L.B. High gamma mapping using EEG. Neuroimage 2010, 49:930-938.
19. Dragoi G., Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 2011, 469:397-401.
20. Eeg-Olofsson O. The development of the electroencephalogram in normal adolescents from the age of 16 through 21years. Neuropadiatrie 1971, 3:11-45.
21. Eeg-Olofsson O. Longitudinal developmental course of electrical activity of brain. Brain Dev 1980, 2:33-44.
22. Espinosa J.S., Stryker M.P. Development and plasticity of the primary visual cortex. Neuron 2012, 75:230-249.
23. Faust K. Very local structure in social networks. Sociol Methodol 2007, 37:209-256.
24. Feinberg I., De Bie E., Davis N.M., Campbell I.G. Topographic differences in the adolescent maturation of the slow wave EEG during NREM sleep. Sleep 2011, 34(325):333.
25. Fifer W.P., Byrd D.L., Kaku M., Eigsti I.M., Isler J.R., Grose-Fifer J., et al. Newborn infants learn during sleep. Proc Natl Acad Sci USA 2010, 107:10320-10323.
26. Freeman W.J., Rogers L.J., Holmes M.D., Silbergeld D.L. Spatial spectral analysis of human electrocorticograms including the alpha and gamma bands. J Neurosci Methods 2000, 95:111-121.
27. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 2005, 9:474-480.
28. Fritschy J.M. Epilepsy, E/I balance and GABA (A) receptor plasticity. Front Mol Neurosci 2008, 1:5.
29. Gais S., Mölle M., Helms K., Born J. Learning-dependent increases in sleep spindle density. J Neurosci 2002, 22:6830-6834.
30. Gasser T., Schuller J.C., Gasser U.S. Correction of muscle artefacts in the EEG power spectrum. Clin Neurophys 2005, 116:2044-2050.
31. Gaudreau H., Carrier J., Montplaisir J. Age-related modifications of NREM sleep EEG: from childhood to middle age. J Sleep Res 2001, 10:165-172.
32. Gray C.M., König P., Engel A.K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 1989, 338:334.
33. He B.J., Raichle M.E. The fMRI signal, slow cortical potential and consciousness. Trends Cogn Sci 2009, 13:302-309.
34. Hensch T.K. Critical period plasticity in local cortical circuits. Nat Rev Neurosci 2005, 11:877-888.
35. Hermoye L., Saint-Martin C., Cosnard G., Lee S.K., Kim J., Nassogne M.C., et al. Pediatric DTI: normal database and observation of the white matter maturation in early childhood. Neuroimage 2006, 29:493-504.
36. Hesdorffer D.C., Logroscino G., Cascino G., Annegers J.F., Hauser W.A. Risk of unprovoked seizure after acute symptomatic seizure: effect of status epilepticus. Ann Neurol 1988, 908-912.
37. Hipp J.F., Engel A.K., Siegel M. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 2011, 69:387-396.
38. Huttenlocher P.R., Dabholkar A.S. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 1997, 387:167-178.
39. Jenni O.G., Carskadon M.A. Spectral analysis of the sleep electroencephalogram during adolescence. Sleep 2004, 27:774-783.
40. Jenni O.G., van Reen E., Carskadon M.A. Regional differences of the sleep electroencephalogram in adolescents. J Sleep Res 2005, 14:141-147.
41. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
42. Khazipov R., Sirota A., Leinekugel X., Holmes G.L., Ben-Ari Y., Buzsaki G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 2004, 432(9):758-761.
43. Komuro H., Rakic P. Modulation of neuronal migration by NMDA receptors. Science 1993, 260:95-97.
44. Kramer M.A., Eden U.T., Cash S.S., Kolaczyk E.D. Network inference with confidence from multivariate time series. Phys Rev E Stat Nonlin Soft Matter Phys 2009, 79:061916.
45. Kramer M.A., Cash S.S. Epilepsy as a disorder of cortical network organization. Neuroscientist 2012, 18:360-372.
46. Kriegstein A.R. Constructing circuits: neurogenesis and migration in the developing neocortex. Epilepsia 2005, 46:15-21.
47. Kuks J.B., Vos J.E., O'Brien M.J. EEG coherence functions for normal newborns in relation to their sleep state. Electroencephalogr Clin Neurophysiol 1988, 69:295-302.
48. Kurth S., Ringli M., Geiger A., LeBourgeois M., Jenni O.G., Huber R. Mapping of cortical activity in the first two decades of life: a high-density sleep electroencephalogram study. J Neurosci 2010, 30:13211-13219.
49. Law S.K. Thickness and resistivity variations over the upper surface of the human skull. Brain Topogr 1993, 6:99-109.
50. Le Magueresse C., Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 2013, 77:388-405.
51. McMenamin B.W., Chackman A.J., Gerischar L.L., Davidson R.J. Electromyogenic artifacts and electroencephalographic inferences revisited. Neuroimage 2011, 54:4-9.
52. Mitra P., Boki H. Observed Brain Dynamics 2007, Oxford University Press, USA.
53. Muthukumaraswamy S.D. High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front Hum Neurosci 2013, 7:1-11.
54. Myers M.M., Grieve P.G., Israelit A., Fifer W.P., Isler J.R., Darnall R.A., et al. Developmental profiles of infant EEG: overlap with transient cortical circuits. Clin Neurophys 2012, 123:1502-1511.
55. Newman M. Networks: an introduction 2010, Oxford University Press, USA. 1st ed.
56. Piantoni G., Astill R.G., Raymann R.J.E.M., Vis J.C., Coppens J.E., Someren E.J.W.V. Modulation of gamma and spindle-range power by slow oscillations in scalp sleep EEG of children. Int J Psychophys 2013, 89:252-258.
57. Nunez P.L., Srinivasan R. Electric fields of the brain: the neurophysics of EEG 2006, Oxford University Press, Oxford.
58. Nunez P.L., Srinivasan R. Scale and frequency chauvinism in brain dynamics: too much emphasis on gamma band oscillations. Brain Struct Funct 2010, 215:67-71.
59. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
60. Partha M., Hemant B. Observed brain dynamics 2008, Oxford University Press, New York.
61. Rosenberg R.S., Van Hout S. The American Academy of Sleep Medicine inter-scorer reliability program: sleep stage scoring. J Clin Sleep Med 2013, 9:81-87.
62. Roux F., Wibral M., Mohr H.M., Singer W., Uhlhaas P.J. Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory. J Neurosci 2012, 32:12411-12420.
63. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010, 52:1059-1069.
64. Sankupellay M., Wilson S., Heussler H.S., Parsley C., Yuill M., Dakin C. Characteristics of sleep EEG power spectra in healthy infants in the first two years of life. Clin Neurophys 2011, 122:236-243.
65. Scher M.S. Ontogeny of EEG-sleep from neonatal through infancy periods. Sleep Med 2008, 9:615-636.
66. Scher M.S., Loparo K.A. Neonatal EEG/sleep state analyses: a complex phenotype of developmental neural plasticity. Dev Neurosci 2009, 31:259-275.
67. Shinnar S., Glauser T. Febrile seizures. J Child Neurol 2002, 17:S44-S52.
68. Silber M.H., Ancoli-Israel S., Bonnet M.H., Chokroverty S., Grigg-Damberger M.M., Hirshkowitz M., et al. The visual scoring of sleep in adults. J Clin Sleep Med 2007, 3:121-131.
69. Singer W. Neuronal synchrony: a versatile code for the definition of relations?. Neuron 1999, 24(49-65):111-125.
70. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006, 137:1087-1106.
71. Smit D.J., Boersma M., Schnack H.G., Micheloyannis S., Boomsma D.I., Hulshoff Pol H.E., et al. The brain matures with stronger functional connectivity and decreased randomness of its network. PLoS One 2012, 7:e36896.
72. Sterman M.B., Harper R.M., Havens B., Hoppenbrouwers T., McGinty D.J., Hodgman J.E. Quantitative analysis of infant EEG development during quiet sleep. Electroencephalogr Clin Neurophysiol 1977, 43:371-385.
73. Stickgold R. Sleep-dependent memory consolidation. Nature 2005, 437:1272-1278.
74. Sun L., Grützner C., Bölte S., Wibral M., Tozman T., Schlitt S., et al. Impaired gamma-band activity during perceptual organization in adults with autism spectrum disorders: evidence for dysfunctional network activity in frontal-posterior cortices. J Neurosci 2012, 11(32):9563-9573.
75. Tarokh L., Carskadon M.A., Achermann P. Developmental changes in brain connectivity assessed using the sleep EEG. Neuroscience 2010, 171:622-634.
76. Tarokh L., Van Reen E., LeBourgeois M., Seifer R., Carskadon M.A. Sleep EEG provides evidence that cortical changes persist into late adolescence. Sleep 2011, 34:1385-1393.
77. Uhlhaas P.J., Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006, 52:155-168.
78. Uhlhaas P.J., Roux F., Singer W., Haenschel C., Sireteanu R., Rodriguez E. The development of neural synchrony reflects late maturation and restricting of functional networks. PNAS 2009, 106:9866-9871.
79. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010, 11:100-113.
80. Boersma M, Smit DJ, de Bie HM, Van Baal GC, Boomsma DI, de Geus EJ, et al. Network analysis of resting state EEG in the developing young brain: structure comes with maturation. Hum Brain Mapp 2011;32:413-25.
81. Gasser T, Verleger R, Bächer P. Sroka. Development of the EEG of school-age children and adolescents. I. Analysis of band power. Electroencephalogr Clin Neurophysiol 1988;69:91-9.
82. He BJ, Zempel JM, Snyder AZ, Raichle ME. The temporal structures and functional significance of scale-free brain activity. Neuron 2010;66:353-69
83. Micheloyannis S, Vourkas M, Tsirka V, Karakonstantaki E, Kanatsouli K, Stam CJ. The influence of ageing on complex brain networks: a graph theoretical analysis. Hum Brain Mapp 2009;30:200-8.
84. Thatcher RW, North DM, Biver CJ. Development of cortical connections as measured by EEG coherence and phase delays. Hum Brain Mapp 2008;29:1400-15.