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

被引:55
作者
Goldstone, Aimee [1 ]
Willoughby, Adrian R. [1 ]
de Zambotti, Massimiliano [1 ]
Franzen, Peter L. [2 ]
Kwon, Dongjin [1 ,3 ]
Pohl, Kilian M. [1 ,3 ]
Pfefferbaum, Adolf [1 ,3 ]
Sullivan, Edith V. [3 ]
Muller-Oehring, Eva M. [1 ,3 ]
Prouty, Devin E. [1 ]
Hasler, Brant P. [2 ]
Clark, Duncan B. [2 ]
Colrain, Ian M. [1 ,4 ]
Baker, Fiona C. [1 ,5 ]
机构
[1] SRI Int, Ctr Hlth Sci, 333 Ravenswood Ave, Menlo Pk, CA 94025 USA
[2] Univ Pittsburgh, Sch Med, Pittsburgh, PA USA
[3] Stanford Univ, Sch Med, Dept Psychiat & Behav Sci, Stanford, CA 94305 USA
[4] Univ Melbourne, Melbourne Sch Psychol Sci, Parkville, Vic, Australia
[5] Univ Witwatersrand, Sch Physiol, Brain Funct Res Grp, Johannesburg, South Africa
关键词
Slow-wave activity; Adolescence; Cortical development; Sleep; HUMAN CEREBRAL-CORTEX; LESS-THAN-1 HZ OSCILLATION; SURFACE-BASED ANALYSIS; DEVELOPMENTAL-CHANGES; IN-VIVO; GEOMETRICALLY ACCURATE; NATIONAL CONSORTIUM; PREFRONTAL CORTEX; BRAIN MATURATION; FREQUENCY BANDS;
D O I
10.1007/s00429-017-1509-9
中图分类号
R602 [外科病理学、解剖学]; R32 [人体形态学];
学科分类号
100101 ;
摘要
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.
引用
收藏
页码:669 / 685
页数:17
相关论文
共 103 条
[11]   Sex Matters during Adolescence: Testosterone-Related Cortical Thickness Maturation Differs between Boys and Girls [J].
Bramen, Jennifer E. ;
Hranilovich, Jennifer A. ;
Dahl, Ronald E. ;
Chen, Jessie ;
Rosso, Carly ;
Forbes, Erika E. ;
Dinov, Ivo D. ;
Worthman, Carol M. ;
Sowell, Elizabeth R. .
PLOS ONE, 2012, 7 (03)
[12]   Puberty Influences Medial Temporal Lobe and Cortical Gray Matter Maturation Differently in Boys Than Girls Matched for Sexual Maturity [J].
Bramen, Jennifer E. ;
Hranilovich, Jennifer A. ;
Dahl, Ronald E. ;
Forbes, Erika E. ;
Chen, Jessica ;
Toga, Arthur W. ;
Dinov, Ivo D. ;
Worthman, Carol M. ;
Sowell, Elizabeth R. .
CEREBRAL CORTEX, 2011, 21 (03) :636-646
[13]   The National Consortium on Alcohol and Neuro-Development in Adolescence (NCANDA): A Multisite Study of Adolescent Development and Substance Use [J].
Brown, Sandra A. ;
Brumback, T. Y. ;
Tomlinson, Kristin ;
Cummins, Kevin ;
Thompson, Wesley K. ;
Nagel, Bonnie J. ;
De Bellis, Michael D. ;
Hooper, Stephen R. ;
Clark, Duncan B. ;
Chung, Tammy ;
Hasler, Brant P. ;
Colrain, Ian M. ;
Baker, Fiona C. ;
Prouty, Devin ;
Pfefferbaum, Adolf ;
Sullivan, Edith V. ;
Pohl, Kilian M. ;
Rohlfing, Torsten ;
Nichols, B. Nolan ;
Chu, Weiwei ;
Tapert, Susan F. .
JOURNAL OF STUDIES ON ALCOHOL AND DRUGS, 2015, 76 (06) :895-908
[14]   Anatomical markers of sleep slow wave activity derived from structural magnetic resonance images [J].
Buchmann, Andreas ;
Kurth, Salome ;
Ringli, Maya ;
Geiger, Anja ;
Jenni, Oskar G. ;
Huber, Reto .
JOURNAL OF SLEEP RESEARCH, 2011, 20 (04) :506-513
[15]   EEG Sleep Slow-Wave Activity as a Mirror of Cortical Maturation [J].
Buchmann, Andreas ;
Ringli, Maya ;
Kurth, Salome ;
Schaerer, Margot ;
Geiger, Anja ;
Jenni, Oskar G. ;
Huber, Reto .
CEREBRAL CORTEX, 2011, 21 (03) :607-615
[16]   A NEW, SEMISTRUCTURED PSYCHIATRIC INTERVIEW FOR USE IN GENETIC-LINKAGE STUDIES - A REPORT ON THE RELIABILITY OF THE SSAGA [J].
BUCHOLZ, KK ;
CADORET, R ;
CLONINGER, CR ;
DINWIDDIE, SH ;
HESSELBROCK, VM ;
NURNBERGER, JI ;
REICH, T ;
SCHMIDT, I ;
SCHUCKIT, MA .
JOURNAL OF STUDIES ON ALCOHOL, 1994, 55 (02) :149-158
[17]   Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation [J].
Campbell, Ian G. ;
Grimm, Kevin J. ;
de Bie, Evan ;
Feinberg, Irwin .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2012, 109 (15) :5740-5743
[18]   Adolescent Changes in Homeostatic Regulation of EEG Activity in the Delta and Theta Frequency Bands during NREM Sleep [J].
Campbell, Ian G. ;
Darchia, Nato ;
Higgins, Lisa M. ;
Dykan, Igor V. ;
Davis, Nicole M. ;
de Bie, Evan ;
Feinberg, Irwin .
SLEEP, 2011, 34 (01) :83-U89
[19]   Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation [J].
Campbell, Ian G. ;
Feinberg, Irwin .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (13) :5177-5180
[20]  
Casey BJ, 2008, DEV REV, V28, P62, DOI [10.1016/j.dr.2007.08.003, 10.1196/annals.1440.010]