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Brain Structure and Function

, Volume 223, Issue 2, pp 669–685 | Cite as

The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence

  • Aimée Goldstone
  • Adrian R. Willoughby
  • Massimiliano de Zambotti
  • Peter L. Franzen
  • Dongjin Kwon
  • Kilian M. Pohl
  • Adolf Pfefferbaum
  • Edith V. Sullivan
  • Eva M. Müller-Oehring
  • Devin E. Prouty
  • Brant P. Hasler
  • Duncan B. Clark
  • Ian M. Colrain
  • Fiona C. Baker
Original Article

Abstract

During the course of adolescence, reductions occur in cortical thickness and gray matter (GM) volume, along with a 65% reduction in slow-wave (delta) activity during sleep (SWA) but empirical data linking these structural brain and functional sleep differences, is lacking. Here, we investigated specifically whether age-related differences in cortical thickness and GM volume and cortical thickness accounted for the typical age-related difference in slow-wave (delta) activity (SWA) during sleep. 132 healthy participants (age 12–21 years) from the National Consortium on Alcohol and NeuroDevelopment in Adolescence study were included in this cross-sectional analysis of baseline polysomnographic, electroencephalographic, and magnetic resonance imaging data. By applying mediation models, we identified a large, direct effect of age on SWA in adolescents, which explained 45% of the variance in ultra-SWA (0.3–1 Hz) and 52% of the variance in delta-SWA (1 to <4 Hz), where SWA was lower in older adolescents, as has been reported previously. In addition, we provide evidence that the structure of several, predominantly frontal, and parietal brain regions, partially mediated this direct age effect, models including measures of brain structure explained an additional 3–9% of the variance in ultra-SWA and 4–5% of the variance in delta-SWA, with no differences between sexes. Replacing age with pubertal status in models produced similar results. As reductions in GM volume and cortical thickness likely indicate synaptic pruning and myelination, these results suggest that diminished SWA in older, more mature adolescents may largely be driven by such processes within a number of frontal and parietal brain regions.

Keywords

Slow-wave activity Adolescence Cortical development Sleep 

Notes

Acknowledgements

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank our lab manager, Stephanie Claudatos, and research assistants, David Dresser, David Sugarbaker, Justin Greco, Sarah Inkelis, Lena Kardos, Devika Nair, and Leonardo Rosas, for their effort in collecting data for this project, and all research participants.

Compliance with ethical standards

Conflict of interest

FCB and MdZ have received research grants from Fitbit Inc., Ebb Inc., and International Flavors and Fragrances Inc.

Financial statement

This study was supported by the National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA); grants: AA021690 (DBC), AA021697 (AP + KMP), AA021697-04S1 (KMP), AA021696 (IMC + FCB) and AA021695 (NCANDA Admin).

Supplementary material

429_2017_1509_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Achermann P, Borbely AA (1997) Low-frequency (<1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81(1):213–222PubMedCrossRefGoogle Scholar
  2. Amzica F, Steriade M (1998) Electrophysiological correlates of sleep delta waves. Electroencephalogr Clin Neurophysiol 107(2):69–83PubMedCrossRefGoogle Scholar
  3. Baker FC, Turlington SR, Colrain I (2012) Developmental changes in the sleep electroencephalogram of adolescent boys and girls. J Sleep Res 21(1):59–67. doi: 10.1111/j.1365-2869.2011.00930.x PubMedCrossRefGoogle Scholar
  4. Baker FC, Willoughby AR, de Zambotti M, Franzen PL, Prouty D, Javitz H, Hasler B, Clark DB, Colrain IM (2016) Age-related differences in sleep architecture and electroencephalogram in adolescents in the national consortium on alcohol and neurodevelopment in adolescence sample. Sleep 39(7):1429–1439. doi: 10.5665/sleep.5978 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bava S, Boucquey V, Goldenberg D, Thayer RE, Ward M, Jacobus J, Tapert SF (2011) Sex differences in adolescent white matter architecture. Brain Res 1375:41–48. doi: 10.1016/j.brainres.2010.12.051 PubMedCrossRefGoogle Scholar
  6. Benoit O, Daurat A, Prado J (2000) Slow (0.7–2 Hz) and fast (2–4 Hz) delta components are differently correlated to theta, alpha and beta frequency bands during NREM sleep. Clin Neurophysiol 111(12):2103–2106PubMedCrossRefGoogle Scholar
  7. Bersagliere A, Achermann P (2010) Slow oscillations in human non-rapid eye movement sleep electroencephalogram: effects of increased sleep pressure. J Sleep Res 19(1 Pt 2):228–237. doi: 10.1111/j.1365-2869.2009.00775.x PubMedCrossRefGoogle Scholar
  8. Blakemore SJ, Burnett S, Dahl RE (2010) The role of puberty in the developing adolescent brain. Hum Brain Mapp 31(6):926–933. doi: 10.1002/hbm.21052 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Borbely AA (1982) A two process model of sleep regulation. Hum Neurobiol 1(3):195–204PubMedGoogle Scholar
  10. Bourgeois JP, Goldman-Rakic PS, Rakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4(1):78–96PubMedCrossRefGoogle Scholar
  11. Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW, Dinov ID, Worthman CM, Sowell ER (2011) Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex 21(3):636–646. doi: 10.1093/cercor/bhq137 PubMedCrossRefGoogle Scholar
  12. Bramen JE, Hranilovich JA, Dahl RE, Chen J, Rosso C, Forbes EE, Dinov ID, Worthman CM, Sowell ER (2012) Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS One 7(3):e33850. doi: 10.1371/journal.pone.0033850 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brown SA, Brumback T, Tomlinson K, Cummins K, Thompson WK, Nagel BJ, De Bellis MD, Hooper SR, Clark DB, Chung T, Hasler BP, Colrain IM, Baker FC, Prouty D, Pfefferbaum A, Sullivan EV, Pohl KM, Rohlfing T, Nichols BN, Chu W, Tapert SF (2015) The National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA): a multisite study of adolescent development and substance use. J Stud Alcohol Drugs 76(6):895–908PubMedPubMedCentralCrossRefGoogle Scholar
  14. Buchmann A, Kurth S, Ringli M, Geiger A, Jenni OG, Huber R (2011a) Anatomical markers of sleep slow wave activity derived from structural magnetic resonance images. J Sleep Res 20(4):506–513. doi: 10.1111/j.1365-2869.2011.00916.x PubMedCrossRefGoogle Scholar
  15. Buchmann A, Ringli M, Kurth S, Schaerer M, Geiger A, Jenni OG, Huber R (2011b) EEG sleep slow-wave activity as a mirror of cortical maturation. Cereb Cortex 21(3):607–615. doi: 10.1093/cercor/bhq129 PubMedCrossRefGoogle Scholar
  16. Bucholz KK, Cadoret R, Cloninger CR, Dinwiddie SH, Hesselbrock VM, Nurnberger JI Jr, Reich T, Schmidt I, Schuckit MA (1994) A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. J Stud Alcohol 55(2):149–158PubMedCrossRefGoogle Scholar
  17. Campbell IG, Feinberg I (2009) Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc Natl Acad Sci USA 106(13):5177–5180. doi: 10.1073/pnas.0812947106 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Campbell IG, Darchia N, Higgins LM, Dykan IV, Davis NM, de Bie E, Feinberg I (2011) Adolescent changes in homeostatic regulation of EEG activity in the delta and theta frequency bands during NREM sleep. Sleep 34(1):83–91PubMedPubMedCentralCrossRefGoogle Scholar
  19. Campbell IG, Grimm KJ, de Bie E, Feinberg I (2012) Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation. Proc Natl Acad Sci USA 109(15):5740–5743. doi: 10.1073/pnas.1120860109 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Casey BJ, Jones RM, Hare TA (2008) The adolescent brain. Ann N Y Acad Sci 1124:111–126. doi: 10.1196/annals.1440.010 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22(4):487–497PubMedCrossRefGoogle Scholar
  22. Colrain IM, Baker FC (2011) Sleep EEG, the clearest window through which to view adolescent brain development. Sleep 34(10):1287–1288. doi: 10.5665/sleep.1260 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9(2):179–194. doi: 10.1006/nimg.1998.0395 PubMedCrossRefGoogle Scholar
  24. Dang-Vu TT, Schabus M, Desseilles M, Albouy G, Boly M, Darsaud A, Gais S, Rauchs G, Sterpenich V, Vandewalle G, Carrier J, Moonen G, Balteau E, Degueldre C, Luxen A, Phillips C, Maquet P (2008) Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci USA 105(39):15160–15165. doi: 10.1073/pnas.0801819105 PubMedPubMedCentralCrossRefGoogle Scholar
  25. de Zambotti M, Colrain IM, Baker FC (2015) Interaction between reproductive hormones and physiological sleep in women. J Clin Endocrinol Metab 100(4):1426–1433. doi: 10.1210/jc.2014-3892 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21. doi: 10.1016/j.jneumeth.2003.10.009 PubMedCrossRefGoogle Scholar
  27. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980. doi: 10.1016/j.neuroimage.2006.01.021 PubMedCrossRefGoogle Scholar
  28. Destexhe A, Contreras D, Steriade M (1999) Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J Neurosci 19(11):4595–4608PubMedGoogle Scholar
  29. Dube J, Lafortune M, Bedetti C, Bouchard M, Gagnon JF, Doyon J, Evans AC, Lina JM, Carrier J (2015) Cortical thinning explains changes in sleep slow waves during adulthood. J Neurosci 35(20):7795–7807. doi: 10.1523/jneurosci.3956-14.2015 PubMedCrossRefGoogle Scholar
  30. Esser SK, Hill SL, Tononi G (2007) Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 30(12):1617–1630PubMedPubMedCentralCrossRefGoogle Scholar
  31. Feinberg I, Campbell IG (2010) Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn 72(1):56–65. doi: 10.1016/j.bandc.2009.09.008 PubMedCrossRefGoogle Scholar
  32. Feinberg I, Campbell IG (2013) Longitudinal sleep EEG trajectories indicate complex patterns of adolescent brain maturation. Am J Physiol Regul Integr Comp Physiol 304(4):R296–R303. doi: 10.1152/ajpregu.00422.2012 PubMedCrossRefGoogle Scholar
  33. Feinberg I, Hibi S, Carlson VR (1977) Changes in EEG amplitude during sleep with age. In: Nandy K, Sherwin I (eds) The aging brain and senile dementia. Springer, US, Boston, pp 85–98CrossRefGoogle Scholar
  34. Feinberg I, Thode HC Jr, Chugani HT, March JD (1990) Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. J Theor Biol 142(2):149–161PubMedCrossRefGoogle Scholar
  35. Feinberg I, Higgins LM, Khaw WY, Campbell IG (2006) The adolescent decline of NREM delta, an indicator of brain maturation, is linked to age and sex but not to pubertal stage. Am J Physiol Regul Integr Comp Physiol 291(6):R1724–R1729. doi: 10.1152/ajpregu.00293.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Feinberg I, de Bie E, Davis NM, Campbell IG (2011) Topographic differences in the adolescent maturation of the slow wave EEG during NREM sleep. Sleep 34(3):325–333PubMedPubMedCentralCrossRefGoogle Scholar
  37. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97(20):11050–11055. doi: 10.1073/pnas.200033797 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9(2):195–207. doi: 10.1006/nimg.1998.0396 PubMedCrossRefGoogle Scholar
  39. Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8(4):272–284PubMedCrossRefGoogle Scholar
  40. Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20(1):70–80. doi: 10.1109/42.906426 PubMedCrossRefGoogle Scholar
  41. Glasser MF, Goyal MS, Preuss TM, Raichle ME, Van Essen DC (2014) Trends and properties of human cerebral cortex: correlations with cortical myelin content. Neuroimage 93(Pt 2):165–175. doi: 10.1016/j.neuroimage.2013.03.060 PubMedCrossRefGoogle Scholar
  42. Gogtay N, Thompson PM (2010) Mapping gray matter development: implications for typical development and vulnerability to psychopathology. Brain Cogn 72(1):6. doi: 10.1016/j.bandc.2009.08.009 PubMedCrossRefGoogle Scholar
  43. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF 3rd, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101(21):8174–8179. doi: 10.1073/pnas.0402680101 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Goldman-Rakic PS (1987) Development of cortical circuitry and cognitive function. Child Dev 58:601–622PubMedCrossRefGoogle Scholar
  45. Hagenauer MH, Lee TM (2012) The neuroendocrine control of the circadian system: adolescent chronotype. Front Neuroendocrinol 33(3):211–229. doi: 10.1016/j.yfrne.2012.04.003 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hagenauer MH, Lee TM (2013) Adolescent sleep patterns in humans and laboratory animals. Horm Behav 64(2):270–279. doi: 10.1016/j.yhbeh.2013.01.013 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hammelrath L, Skokic S, Khmelinskii A, Hess A, van der Knaap N, Staring M, Lelieveldt BP, Wiedermann D, Hoehn M (2016) Morphological maturation of the mouse brain: an in vivo MRI and histology investigation. Neuroimage 125:144–152. doi: 10.1016/j.neuroimage.2015.10.009 PubMedCrossRefGoogle Scholar
  48. Hanlon EC, Vyazovskiy VV, Faraguna U, Tononi G, Cirelli C (2011) Synaptic potentiation and sleep need: clues from molecular and electrophysiological studies. Curr Top Med Chem 11(19):2472–2482PubMedCrossRefGoogle Scholar
  49. Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. Guilford Press, New YorkGoogle Scholar
  50. Herting MM, Maxwell EC, Irvine C, Nagel BJ (2012) The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb Cortex 22(9):1979–1992. doi: 10.1093/cercor/bhr246 PubMedCrossRefGoogle Scholar
  51. Herting MM, Gautam P, Spielberg JM, Kan E, Dahl RE, Sowell ER (2014) The role of testosterone and estradiol in brain volume changes across adolescence: a longitudinal structural MRI study. Hum Brain Mapp 35(11):5633–5645. doi: 10.1002/hbm.22575 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Herting MM, Gautam P, Spielberg JM, Dahl RE, Sowell ER (2015) A longitudinal study: changes in cortical thickness and surface area during pubertal maturation. PLoS One 10(3):e0119774. doi: 10.1371/journal.pone.0119774 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Huttenlocher PR (1979) Synaptic density in human frontal cortex—developmental changes and effects of aging. Brain Res 163(2):195–205PubMedCrossRefGoogle Scholar
  54. Jenni OG, Carskadon MA (2004) Spectral analysis of the sleep electroencephalogram during adolescence. Sleep 27(4):774–783PubMedGoogle Scholar
  55. Jernigan TL, Trauner DA, Hesselink JR, Tallal PA (1991) Maturation of human cerebrum observed in vivo during adolescence. Brain 114(Pt 5):2037–2049PubMedCrossRefGoogle Scholar
  56. Jernigan TL, Brown TT, Bartsch H, Dale AM (2016) Toward an integrative science of the developing human mind and brain: focus on the developing cortex. Dev Cogn Neurosci 18:2–11. doi: 10.1016/j.dcn.2015.07.008 PubMedCrossRefGoogle Scholar
  57. Judd CM, Kenny DA (1981) Process analysis: estimating mediation in treatment evaluations. Eval Rev 5(5):602–619CrossRefGoogle Scholar
  58. Judd CM, Kenny DA, McClelland GH (2001) Estimating and testing mediation and moderation in within-subject designs. Psychol Methods 6(2):115–134PubMedCrossRefGoogle Scholar
  59. Kassem MS, Lagopoulos J, Stait-Gardner T, Price WS, Chohan TW, Arnold JC, Hatton SN, Bennett MR (2013) Stress-induced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses. Mol Neurobiol 47(2):645–661. doi: 10.1007/s12035-012-8365-7 PubMedCrossRefGoogle Scholar
  60. Kennedy C, Sokoloff L (1957) An adaptation of the nitrous oxide method to the study of the cerebral circulation in children; normal values for cerebral blood flow and cerebral metabolic rate in childhood. J Clin Investig 36(7):1130–1137. doi: 10.1172/jci103509 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Keshavan MS, Anderson S, Pettergrew JW (1994) Is Schizophrenia due to excessive synaptic pruning in the prefrontal cortex? The Feinberg hypothesis revisited. J Psychiatr Res 28(3):239–265. doi: 10.1016/0022-3956(94)90009-4 PubMedCrossRefGoogle Scholar
  62. Knyazev GG (2012) EEG delta oscillations as a correlate of basic homeostatic and motivational processes. Neurosci Biobehav Rev 36(1):677–695. doi: 10.1016/j.neubiorev.2011.10.002 PubMedCrossRefGoogle Scholar
  63. Le Bon O, Linkowski P (2013) Absence of systematic relationships between REMS duration episodes and spectral power Delta and Ultra-Slow bands in contiguous NREMS episodes in healthy humans. J Neurophysiol 110(1):162–169. doi: 10.1152/jn.00020.2013 PubMedCrossRefGoogle Scholar
  64. Le Bon O, Neu D, Berquin Y, Lanquart JP, Hoffmann R, Mairesse O, Armitage R (2012) Ultra-slow delta power in chronic fatigue syndrome. Psychiatry Res 200(2–3):742–747. doi: 10.1016/j.psychres.2012.06.027 PubMedCrossRefGoogle Scholar
  65. Lenroot RK, Giedd JN (2010) Sex differences in the adolescent brain. Brain Cogn 72(1):46. doi: 10.1016/j.bandc.2009.10.008 PubMedCrossRefGoogle Scholar
  66. Lopes da Silva FH, van Rotterdam A (2005) Biophysical aspects of EEG and magnetoencephalographic generation. In: Niedermeyer E, Lopes da Silva F (eds) Electroencephalography: basic principles, clinical applications and related fields, 5th edn. Lippincott, Williams & Wilkins, New YorkGoogle Scholar
  67. Lopes da Silva FH (2010) EEG: origin and measurement. In: Mulert C, Lemieux L (eds) EEG-fMRI: physiological basis, technique, and applications. Springer, Berlin, Heidelberg, pp 19–38Google Scholar
  68. MacKinnon DP, Fairchild AJ, Fritz MS (2007) Mediation analysis. Annu Rev Psychol 58:593–614. doi: 10.1146/annurev.psych.58.110405.085542 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mengler L, Khmelinskii A, Diedenhofen M, Po C, Staring M, Lelieveldt BP, Hoehn M (2014) Brain maturation of the adolescent rat cortex and striatum: changes in volume and myelination. Neuroimage 84:35–44. doi: 10.1016/j.neuroimage.2013.08.034 PubMedCrossRefGoogle Scholar
  70. Mills KL, Goddings A-L, Herting MM, Meuwese R, Blakemore S-J, Crone EA, Dahl RE, Güroğlu B, Raznahan A, Sowell ER, Tamnes CK (2016) Structural brain development between childhood and adulthood: convergence across four longitudinal samples. Neuroimage 141:273–281. doi: 10.1016/j.neuroimage.2016.07.044 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Moroni F, Nobili L, Iaria G, Sartori I, Marzano C, Tempesta D, Proserpio P, Lo Russo G, Gozzo F, Cipolli C, De Gennaro L, Ferrara M (2014) Hippocampal slow EEG frequencies during NREM sleep are involved in spatial memory consolidation in humans. Hippocampus 24(10):1157–1168. doi: 10.1002/hipo.22299 PubMedCrossRefGoogle Scholar
  72. Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G (2009) Source modeling sleep slow waves. Proc Natl Acad Sci USA 106(5):1608–1613. doi: 10.1073/pnas.0807933106 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Nichols BN, Pohl KM (2015) Neuroinformatics software applications supporting electronic data capture, management, and sharing for the neuroimaging community. Neuropsychol Rev 25(3):356–368. doi: 10.1007/s11065-015-9293-x PubMedPubMedCentralCrossRefGoogle Scholar
  74. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  75. Perrault R, Carrier J, Desautels A, Montplaisir J, Zadra A (2014) Electroencephalographic slow waves prior to sleepwalking episodes. Sleep Med 15(12):1468–1472. doi: 10.1016/j.sleep.2014.07.020 PubMedCrossRefGoogle Scholar
  76. Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 17(2):117–133. doi: 10.1007/bf01537962 PubMedCrossRefGoogle Scholar
  77. Pfefferbaum A, Rohlfing T, Pohl KM, Lane B, Chu W, Kwon D, Nolan Nichols B, Brown SA, Tapert SF, Cummins K, Thompson WK, Brumback T, Meloy MJ, Jernigan TL, Dale A, Colrain IM, Baker FC, Prouty D, De Bellis MD, Voyvodic JT, Clark DB, Luna B, Chung T, Nagel BJ, Sullivan EV (2015) Adolescent development of cortical and white matter structure in the NCANDA sample: role of sex, ethnicity, puberty, and alcohol drinking. Cereb Cortex. doi: 10.1093/cercor/bhv205 Google Scholar
  78. Pinyerd B, Zipf WB (2005) Puberty-timing is everything! J Pediatr Nurs 20(2):75–82. doi: 10.1016/j.pedn.2004.12.011 PubMedCrossRefGoogle Scholar
  79. Pohl KM, Sullivan EV, Rohlfing T, Chu W, Kwon D, Nichols BN, Zhang Y, Brown SA, Tapert SF, Cummins K, Thompson WK, Brumback T, Colrain IM, Baker FC, Prouty D, De Bellis MD, Voyvodic JT, Clark DB, Schirda C, Nagel BJ, Pfefferbaum A (2016) Harmonizing DTI measurements across scanners to examine the development of white matter microstructure in 803 adolescents of the NCANDA study. Neuroimage 130:194–213. doi: 10.1016/j.neuroimage.2016.01.061 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Preacher KJ, Rucker DD, Hayes AF (2007) Addressing moderated mediation hypotheses: theory, methods, and prescriptions. Multivar Behav Res 42(1):185–227CrossRefGoogle Scholar
  81. Ringli M, Kurth S, Huber R, Jenni OG (2013) The sleep EEG topography in children and adolescents shows sex differences in language areas. Int J Psychophysiol 89(2):241–245. doi: 10.1016/j.ijpsycho.2013.04.008 PubMedCrossRefGoogle Scholar
  82. Saletin JM, van der Helm E, Walker MP (2013) Structural brain correlates of human sleep oscillations. Neuroimage 83:658–668. doi: 10.1016/j.neuroimage.2013.06.021 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Schmierer K, Tozer DJ, Scaravilli F, Altmann DR, Barker GJ, Tofts PS, Miller DH (2007) Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J Magn Reson Imaging 26(1):41–51. doi: 10.1002/jmri.20984 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Schuz A, Palm G (1989) Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286(4):442–455. doi: 10.1002/cne.902860404 PubMedCrossRefGoogle Scholar
  85. Segonne F, Pacheco J, Fischl B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 26(4):518–529. doi: 10.1109/tmi.2006.887364 PubMedCrossRefGoogle Scholar
  86. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN, Wise SP (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28(14):3586–3594. doi: 10.1523/jneurosci.5309-07.2008 PubMedCrossRefGoogle Scholar
  87. Shirtcliff EA, Dahl RE, Pollak SD (2009) Pubertal development: correspondence between hormonal and physical development. Child Dev 80(2):327–337. doi: 10.1111/j.1467-8624.2009.01263.x PubMedPubMedCentralCrossRefGoogle Scholar
  88. Sisk CL, Foster DL (2004) The neural basis of puberty and adolescence. Nat Neurosci 7(10):1040–1047. doi: 10.1038/nn1326 PubMedCrossRefGoogle Scholar
  89. Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW (2004a) Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24(38):8223–8231. doi: 10.1523/jneurosci.1798-04.2004 PubMedCrossRefGoogle Scholar
  90. Sowell ER, Thompson PM, Toga AW (2004b) Mapping changes in the human cortex throughout the span of life. Neuroscientist 10(4):372–392. doi: 10.1177/1073858404263960 PubMedCrossRefGoogle Scholar
  91. Steriade M, McCarley R (2005) Brain control of wakefulness and sleeping. Springer, New YorkGoogle Scholar
  92. Steriade M, Contreras D, Curro Dossi R, Nunez A (1993a) The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13(8):3284–3299PubMedGoogle Scholar
  93. Steriade M, Nunez A, Amzica F (1993b) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13(8):3266–3283PubMedGoogle Scholar
  94. Steriade M, Nunez A, Amzica F (1993c) A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13(8):3252–3265PubMedGoogle Scholar
  95. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85(5):1969–1985PubMedCrossRefGoogle Scholar
  96. Sullivan EV, Pfefferbaum A, Rohlfing T, Baker FC, Padilla ML, Colrain IM (2011) Developmental change in regional brain structure over 7 months in early adolescence: comparison of approaches for longitudinal atlas-based parcellation. Neuroimage 57(1):214–224. doi: 10.1016/j.neuroimage.2011.04.003 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sullivan EV, Brumback T, Tapert SF, Fama R, Prouty D, Brown SA, Cummins K, Thompson WK, Colrain IM, Baker FC, De Bellis MD, Hooper SR, Clark DB, Chung T, Nagel BJ, Nichols BN, Rohlfing T, Chu W, Pohl KM, Pfefferbaum A (2016) Cognitive, emotion control, and motor performance of adolescents in the NCANDA study: contributions from alcohol consumption, age, sex, ethnicity, and family history of addiction. Neuropsychology 30(4):449–473. doi: 10.1037/neu0000259 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011:13. doi: 10.1155/2011/879716 CrossRefGoogle Scholar
  99. Tarokh L, Carskadon MA (2010) Developmental changes in the human sleep EEG during early adolescence. Sleep 33(6):801–809PubMedPubMedCentralCrossRefGoogle Scholar
  100. Tarokh L, Saletin JM, Carskadon MA (2016) Sleep in adolescence: physiology, cognition and mental health. Neurosci Biobehav Rev. doi: 10.1016/j.neubiorev.2016.08.008 PubMedPubMedCentralGoogle Scholar
  101. Wagstyl K, Ronan L, Whitaker KJ, Goodyer IM, Roberts N, Crow TJ, Fletcher PC (2016) Multiple markers of cortical morphology reveal evidence of supragranular thinning in schizophrenia. Transl Psychiatry 6:e780. doi: 10.1038/tp.2016.43 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Whitaker KJ, Vertes PE, Romero-Garcia R, Vasa F, Moutoussis M, Prabhu G, Weiskopf N, Callaghan MF, Wagstyl K, Rittman T, Tait R, Ooi C, Suckling J, Inkster B, Fonagy P, Dolan RJ, Jones PB, Goodyer IM, Bullmore ET (2016) Adolescence is associated with genomically patterned consolidation of the hubs of the human brain connectome. Proc Natl Acad Sci USA 113(32):9105–9110. doi: 10.1073/pnas.1601745113 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Willoughby AR, de Zambotti M, Baker FC, Colrain IM (2015) Partial K-complex recovery following short-term abstinence in individuals with alcohol use disorder. Alcohol Clin Exp Res 39(8):1417–1424. doi: 10.1111/acer.12769 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Aimée Goldstone
    • 1
  • Adrian R. Willoughby
    • 1
  • Massimiliano de Zambotti
    • 1
  • Peter L. Franzen
    • 2
  • Dongjin Kwon
    • 1
    • 3
  • Kilian M. Pohl
    • 1
    • 3
  • Adolf Pfefferbaum
    • 1
    • 3
  • Edith V. Sullivan
    • 3
  • Eva M. Müller-Oehring
    • 1
    • 3
  • Devin E. Prouty
    • 1
  • Brant P. Hasler
    • 2
  • Duncan B. Clark
    • 2
  • Ian M. Colrain
    • 1
    • 4
  • Fiona C. Baker
    • 1
    • 5
  1. 1.Centre for Health SciencesSRI InternationalMenlo ParkUSA
  2. 2.University of Pittsburgh School of MedicinePittsburghUSA
  3. 3.Department of Psychiatry and Behavioral SciencesStanford University School of MedicineStanfordUSA
  4. 4.Melbourne School of Psychological SciencesUniversity of MelbourneParkvilleAustralia
  5. 5.Brain Function Research Group, School of PhysiologyUniversity of WitwatersrandJohannesburgSouth Africa

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