Cortical thinning explains changes in sleep slow waves during adulthood

Journal of Neuroscience

Volumn 35, Issue 20, 2015, Pages 7795-7807

  Dubè, Jonathan ^a,b,c   Lafortune, Marjolaine ^b   Bedetti, Christophe ^b,c   Bouchard, Maude ^a,b,c   Gagnon, Jean François ^b,d   Doyon, Julien ^a,c   Evans, Alan C ^e   Lina, Jean Marc ^f,g   Carrier, Julie ^a,b,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^c CENTRE DE RECHERCHE   (Canada)

^d UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f ÉCOLE DE TECHNOLOGIE SUPÉRIEURE   (Canada)

^g Center de Recherches Mathematiques   (Canada)

Author keywords

Aging; Cortical thickness; Electroencephalography; Humans; Sleep; Slow waves

Indexed keywords

ADULT; ADULTHOOD; AGE; AGING; ARTICLE; COGNITION; CORTICAL THICKNESS (BRAIN); ELECTROENCEPHALOGRAPHY; FEMALE; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL NETWORK; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POLYSOMNOGRAPHY; PRIORITY JOURNAL; REM SLEEP; SLEEP TIME; SLOW WAVE SLEEP; AGED; BRAIN CORTEX; ELECTROENCEPHALOGRAM; GROWTH, DEVELOPMENT AND AGING; MIDDLE AGED; PHYSIOLOGY; SLEEP; WHITE MATTER;

ADULT; AGED; BRAIN WAVES; CEREBRAL CORTEX; FEMALE; HUMANS; MALE; MIDDLE AGED; SLEEP; WHITE MATTER;

EID: 84929698386     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3956-14.2015     Document Type: Article

References (57)

1. Ad-Dab’bagh Y, Einarson D, Lyttelton O, Muehlboeck JS, Mok K, Ivanov O, Vincent RD, Lepage C, Lerch J, Fombonne E, Evans AC (2006) The CIVET image-processing environment: a fully automated comprehensive pipeline for anatomical neuroimaging research. In: Proceedings of the 12th Annual Meeting of the Organization for Human Brain Mapping, (Corbetta M, ed.). Florence, Italy, Neuroimage.
2. Aeschbach D, Borbely AA (1993) All-night dynamics of the human sleep EEG. J Sleep Res 2:70-81.CrossRef Medline
3. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders. Washington, DC: APA.
4. Amzica F, Steriade M (1995) Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J Neurosci 15:4658-4677. Medline
5. Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56:893-897.CrossRef Medline
6. Bezzola L, Mèrillat S, Gaser C, Jäncke L (2011) Training-induced neural plasticity in golf novices. J Neurosci 31:12444-12448.CrossRef Medline
7. Brunner DP, Vasko RC, Detka CS, Monahan JP, Reynolds CF III, Kupfer DJ (1996) Muscle artifacts in the sleep EEG: automated detection and effect on all-night EEG power spectra. J Sleep Res 5:155-164.CrossRef Medline
8. 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 20:506-513.CrossRef Medline
9. 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 21:607-615.CrossRef Medline
10. Burzynska AZ, Nagel IE, Preuschhof C, Gluth S, Bäckman L, Li, SC, Lindenberger U, Heekeren HR (2012) Cortical thickness is linked to executive functioning in adulthood and aging. Hum Brain Mapp 33:1607-1620.CrossRef Medline
11. Carrier J, Viens I, Poirier G, Robillard R, Lafortune M, Vandewalle G, Martin N, Barakat M, Paquet J, Filipini D (2011) Sleep slow wave changes during the middle years of life. Eur J Neurosci 33:758-766.CrossRef Medline
12. Chauvette S, Volgushev M, Timofeev I (2010) Origin of active states in local neocortical networks during slow sleep oscillation. Cereb Cortex 20: 2660-2674.CrossRef Medline
13. Collins DL, Peters TM, Evans AC (1994) Automated3Dnonlinear deformation procedure for determination of gross morphometric variability in human brain. Visualization in Biomedical Computing 2359:180-190.
14. 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 U S A 105: 15160-15165.CrossRef Medline
15. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth Ø, Larsen VA, Walhovd KB (2010) Effects of memory training on cortical thickness in the elderly. Neuroimage 52:1667-1676.CrossRef Medline
16. Fiebach CJ, Friederici AD, Smith EE, Swinney D (2007) Lateral inferotemporal cortex maintains conceptual-semantic representations in verbal working memory. J Cogn Neurosci 19:2035-2049.CrossRef Medline
17. Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB (2009) High consistency of regional cortical thinning in aging across multiple samples. Cereb Cortex 19:2001-2012.CrossRef Medline
18. Grabner G, Janke AL, Budge MM, Smith D, Pruessner J, Collins DL (2006) Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Medical image computing and computer-assisted intervention: MICCAI. International Conference on Medical Image Computing and Computer-Assisted Intervention 9:58-66.
19. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545.CrossRef Medline
20. Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis. New York: Guilford.
21. Iber C, Ancoli-Israel S, Chesson A, Quan S (2007) The AASM manual for the scoring of sleep and associated events. Westchester, IL: American Academy of Sleep Medicine.
22. Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab’bagh Y, MacDonald D, Lee JM, Kim SI, Evans AC (2005) Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage 27:210-221.CrossRef Medline
23. Lafortune M, Gagnon JF, Latreille V, Vandewalle G, Martin N, Filipini D, Doyon J, Carrier J (2012) Reduced slow-wave rebound during daytime recovery sleep in middle-aged subjects. PLoS One 7:e43224.CrossRef Medline
24. Lafortune M, Gagnon JF, Martin N, Latreille V, Dube´ J, Bouchard M, Bastien C, Carrier J (2014) Sleep spindles and rapid eye movement sleep as predictors of next morning cognitive performance in healthy middle-aged and older participants. J Sleep Res 23:159-167. Medline
25. Landolt HP, Borbely AA (2001) Age-dependent changes in sleep EEG topography. Clin Neurophysiol 112:369-377.CrossRef Medline
26. Liu ME, Huang CC, Hwang JP, Yang AC, Tu PC, Yeh HL, Hong CJ, Liou YJ, Chen JF, Lin CP, Tsai SJ (2013) Effect of Bcl-2 rs956572 SNP on regional gray matter volumes and cognitive function in elderly males without dementia. AGE 35:343-352. Medline
27. Liu ME, Huang CC, Yang AC, Tu PC, Yeh HL, Hong CJ, Chen JF, Liou YJ, Lin CP, Tsai SJ (2013) Effect of Bcl-2 rs956572 Polymorphism on agerelated gray matter volume changes. PLoS One 8:e56663.CrossRef Medline
28. Luebke JI, Chang YM, Moore TL, Rosene DL (2004) Normal aging results in decreased synaptic excitation and increased synaptic inhibition of layer 2/3 pyramidal cells in the monkey prefrontal cortex. Neuroscience 125: 277-288.CrossRef Medline
29. MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12:340-356.CrossRef Medline
30. Mander BA, Rao V, Lu B, Saletin JM, Lindquist JR, Ancoli-Israel S, Jagust W, Walker MP (2013) Prefrontal atrophy, disruptedNREMslow waves and impaired hippocampal-dependent memory in aging. Nat Neurosci 16: 357-364.CrossRef Medline
31. Marshall L, Helgadottir H, Molle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444:610-613.CrossRef Medline
32. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862-6870.CrossRef Medline
33. Menicucci D, Piarulli A, Debarnot U, d’Ascanio P, Landi A, Gemignani A (2009) Functional structure of spontaneous sleep slow oscillation activity in humans. PLoS One 4:e7601.CrossRef Medline
34. Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G (2009) Source modeling sleep slow waves. Proc Natl Acad Sci U S A 106: 1608-1613.CrossRef Medline
35. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70: 153-169.CrossRef Medline
36. Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947-957. Medline
37. Piantoni G, Poil SS, Linkenkaer-Hansen K, Verweij IM, Ramautar JR, Van Someren EJ, Van Der Werf YD (2013) Individual differences in white matter diffusion affect sleep oscillations. J Neurosci 33:227-233.CrossRef Medline
38. Preacher KJ, Kelley K (2011) Effect size measures for mediation models: quantitative strategies for communicating indirect effects. Psychological Methods 16:93-115.CrossRef Medline
39. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RS, Busa E, Morris JC, Dale AM, Fischl B (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721-730.CrossRef Medline
40. Salat DH, Greve DN, Pacheco JL, Quinn BT, Helmer KG, Buckner RL, Fischl B (2009) Regional white matter volume differences in nondemented aging and Alzheimer’s disease. Neuroimage 44:1247-1258.CrossRef Medline
41. Saletin JM, van der Helm E, Walker MP (2013) Structural brain correlates of human sleep oscillations. Neuroimage 83:658-668.CrossRef Medline
42. Schüz A, Palm G (1989) Density of neurons and synapses in the cerebral cortex of the mouse. J Comp Neurol 286:442-455.CrossRef Medline
43. Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87-97.CrossRef Medline
44. Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087-1106.CrossRef Medline
45. Steriade M, Contreras D, CurroDossi 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 13:3284-3299. Medline
46. Steriade M, Nunez A, Amzica F (1993b) A novel slow (1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252-3265. Medline
47. Tohka J, Zijdenbos A, Evans A (2004) Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 23:84-97.CrossRef Medline
48. Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81:12-34.CrossRef Medline
49. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775-15786.CrossRef Medline
50. van den Heuvel MP, Kahn RS, Goni J, Sporns O (2012) High-cost, highcapacity backbone for global brain communication. Proc Natl Acad Sci U S A 109:11372-11377.CrossRef Medline
51. Volgushev M, Chauvette S, Mukovski M, Timofeev I (2006) Precise longrange synchronization of activity and silence in neocortical neurons during slow-wave oscillations [corrected]. J Neurosci 26:5665-5672.CrossRef Medline
52. Vyazovskiy VV, Harris KD (2013) Sleep and the single neuron: the role of global slow oscillations in individual cell rest. Nat Rev Neurosci 14:443-451. Medline
53. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G (2009) Cortical firing and sleep homeostasis. Neuron 63:865-878.CrossRef Medline
54. Wester JC, Contreras D (2012) Columnar interactions determine horizontal propagation of recurrent network activity in neocortex. J Neurosci 32:5454-5471.CrossRef Medline
55. Wong TP, Marchese G, Casu MA, Ribeiro-da-Silva A, Cuello AC, De Koninck Y (2006) Imbalance towards inhibition as a substrate of agingassociated cognitive impairment. Neurosci Lett 397:64-68.CrossRef Medline
56. Worsley KJ, Taylor JE, Tomaiuolo F, Lerch J (2004) Unified univariate and multivariate random field theory. Neuroimage 23:S189-S195.CrossRef Medline
57. Zhao L, Boucher M, Rosa-Neto P, Evans AC (2013) Impact of scale space search on age-and gender-related changes in MRI-based cortical morphometry. Hum Brain Mapp 34:2113-2128.CrossRef Medline