Localizing Age-Related Changes in Brain Structure between Childhood and Adolescence Using Statistical Parametric Mapping
Abstract
Volumetric studies have consistently shown reductions in cerebral gray matter volume between childhood and adolescence, with the most dramatic changes occurring in the more dorsal cortices of the frontal and parietal lobes. The purpose of this study was to examine the spatial location of these changes employing methods typical of functional imaging studies. T1-weighted structural MRI data (1.2 mm) were analyzed for nine normally developing children and nine normal adolescents. Validity and reliability of the tissue segmentation protocol were assessed as part of several preprocessing analyses prior to statistical parametric mapping (SPM). Using SPM96, a simple contrast of average gray matter differences between the two age groups revealed 57 significant clusters (SPM[Z] height threshold, P<0.001, extent threshold 50, uncorrected). The pattern and distribution of differences were consistent with earlier findings from the volumetric assessment of the same subjects. Specifically, more differences were observed in dorsal frontal and parietal regions with relatively few differences observed in cortices of the temporal and occipital lobes. Permutation tests were conducted to assess the overall significance of the gray matter differences and validity of the parametric maps. Twenty SPMs were created with subjects randomly assigned to groups. None of the random SPMs approached the number of significant clusters observed in the age difference SPM (mean number of significant clusters = 5.8). The age effects observed appear to result from regions that consistently segment as gray matter in the younger group and consistently segment as white matter in the older group. The utility of these methods for localizing relatively subtle structural changes that occur between childhood and adolescence has not previously been examined.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Changing cortical volumes over the adolescent age range are most prominent in the frontal and parietal lobes.
“Interestingly, changing cortical volumes over this age range are most prominent in the frontal and parietal lobes.8, 58, 59”
From A role for synaptic plasticity in the adolescent development of executive function (2013) · cites this paper as [59]
In an MRI study comparing children of average age 9 and adolescents of average age 14, older children had higher white matter volume in frontal and parietal cortex, while younger children had higher grey matter volume in the same regions.
“The results showed a higher volume of white matter in the frontal cortex and parietal cortex in the older children than in the younger group.The younger group, by contrast, had a higher volume of grey matter in the same regions.”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Sowell et al., 1999
Absolute prefrontal cortex volume declines during adolescence in both humans and rats.
“absolute PFC volume declines during adolescence in both humans (Sowell et al., 2001; Sowell et al., 1999) and rats (van Eden et al., 1990).”
From Impulsivity, frontal lobes and risk for addiction (2009) · cites this paper as Sowell et al., 1999
Grey matter density in the frontal and temporal lobes follows an inverted-U shaped pattern of development.
“Grey matter density in the frontal and temporal lobes has been reported to follow an inverted-U shaped pattern of development, peaking around puberty onset in the frontal lobe (age 11 in girls and 12 in boys), and at around 16–17 years in the temporal lobe.”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sowell et al., 1999
Frontal lobe grey matter density peaks around puberty onset (age 11 in girls and 12 in boys).
“peaking around puberty onset in the frontal lobe (age 11 in girls and 12 in boys)”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sowell et al., 1999
These peaks in grey matter density are followed by an extended profile of decline throughout the remainder of adolescence and early adulthood.
“These peaks in grey matter density are followed by an extended profile of decline throughout the remainder of adolescence and early adulthood (Giedd et al., 1999; Sowell et al., 1999, 2002; Ostby et al., 2009).”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sowell et al., 1999
MRI studies show continuing neuroanatomical development during adolescence.
“MRI studies show continuing neuroanatomical development during adolescence (Giedd et al., 1999; Sowell et al., 1999; Gogtay et al., 2004).”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sowell et al., 1999
Temporal lobe grey matter density peaks around 16-17 years.
“and at around 16–17 years in the temporal lobe”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sowell et al., 1999
Cites
Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space
Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994) · Journal of Computer Assisted Tomography · doi:10.1097/00004728-199403000-00005 · Cited by 3,431 · cited 2× · see citing works
“The filtered, issue-classified supratentorial volume from each subect was then scaled into standard ICBM-305 space sing a completely automated nine-parameter linear with scaling in the x, y, and z planes) spatial normalizaion algorithm (Collins et al., 1994).”
Method
Flagged first, then by citations
Cited by
Sorted by citations
Voxel-Based Morphometry—The Methods
Ashburner, J., & Friston, K. J. (2000) · NeuroImage · doi:10.1006/nimg.2000.0582 · Cited by 8,676 · see citing works
Unbiased average age-appropriate atlases for pediatric studies
Fonov, V., Evans, A. C., Botteron, K., Almli, C. R., McKinstry, R. C., & Collins, D. L. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.033 · Cited by 2,290 · see citing works
Mapping cortical change across the human life span
Sowell, E. R., Peterson, B. S., Thompson, P. M., Welcome, S. E., Henkenius, A. L., & Toga, A. W. (2003) · Nature Neuroscience · doi:10.1038/nn1008 · Cited by 2,328 · see citing works
Self-citationDevelopment of the adolescent brain: implications for executive function and social cognition
Blakemore, S., & Choudhury, S. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01611.x · Cited by 2,328 · see citing works
The basics of brain development
Stiles, J., & Jernigan, T. L. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9148-4 · Cited by 2,009 · see citing works
Self-citationLongitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children
Sowell, E. R., Thompson, P. M., Leonard, C. M., Welcome, S. E., Kan, E., & Toga, A. W. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1798-04.2004 · Cited by 1,481 · see citing works
Self-citationIn vivo evidence for post-adolescent brain maturation in frontal and striatal regions
Sowell, E. R., Thompson, P. M., Holmes, C. J., Jernigan, T. L., & Toga, A. W. (1999) · Nature Neuroscience · doi:10.1038/13154 · Cited by 1,439 · see citing works
Self-citationNormal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391 · see citing works
Adolescent suicide and suicidal behavior
Bridge, J. A., Goldstein, T. R., & Brent, D. A. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01615.x · Cited by 1,361 · see citing works
Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
Sowell, E. R., Thompson, P. M., Tessner, K. D., & Toga, A. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-22-08819.2001 · Cited by 983 · see citing works
“Because the greatest changes in gray matter density occur in the dorsal frontal cortex between adolescence and adulthood (Sowell et al., 1999a), this was the region that we targeted in the permutation analyses (all gray matter brain tissue anterior to the central sulcus and superior to the axial…”
BackgroundResultInfluentialSelf-citationExercise and Children’s Intelligence, Cognition, and Academic Achievement
Tomporowski, P. D., Davis, C. L., Miller, P. H., & Naglieri, J. A. (2008) · Educational Psychology Review · doi:10.1007/s10648-007-9057-0 · Cited by 874 · see citing works
Maturation of white matter in the human brain: A review of magnetic resonance studies.
Paus, T., Collins, D. L., Evans, A. C., Leonard, G., Pike, B., & Zijdenbos, A. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00434-2 · Cited by 863 · see citing works
Toga, A. W., Thompson, P. M., & Sowell, E. R. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.01.007 · Cited by 872 · see citing works
Self-citationEvaluating the theory of executive dysfunction in autism
Hill, E. L. (2004) · Developmental Review · doi:10.1016/j.dr.2004.01.001 · Cited by 846 · see citing works
Traumatic stress: effects on the brain
Bremner, J. D. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/jbremner · Cited by 738 · see citing works
Sowell, E. R., Peterson, B. S., Kan, E., Woods, R. P., Yoshii, J., Bansal, R., Xu, D., Zhu, H., Thompson, P. M., & Toga, A. W. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl066 · Cited by 695 · see citing works
Self-citationA shift from diffuse to focal cortical activity with development
Durston, S., Davidson, M. C., Tottenham, N., Galvan, A., Spicer, J., Fossella, J. A., & Casey, B. J. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2005.00454.x · Cited by 692 · see citing works
Impulsivity, frontal lobes and risk for addiction
Crews, F. T., & Boettiger, C. A. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.018 · Cited by 679 · see citing works
“Major changes occur in brain during adolescence with absolute PFC volume declines during adolescence in both humans (Sowell et al., 2001; Sowell et al., 1999) and rats (van Eden et al.”
BackgroundSowell, E. R., Trauner, D. A., Gamst, A., & Jernigan, T. L. (2002) · Developmental Medicine and Child Neurology · doi:10.1017/s0012162201001591 · Cited by 701 · see citing works
Self-citationImaging brain development: The adolescent brain
Blakemore, S.-J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.080 · Cited by 649 · see citing works
Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., & Brammer, M. (2006) · Human Brain Mapping · doi:10.1002/hbm.20237 · Cited by 632 · see citing works
Johnson, S. B., Blum, R. W., & Giedd, J. N. (2009) · Journal of Adolescent Health · doi:10.1016/j.jadohealth.2009.05.016 · Cited by 631 · see citing works
Nakao, T., Radua, J., Rubia, K., & Mataix-Cols, D. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11020281 · Cited by 588 · see citing works
<scp>N</scp> icotine and the adolescent brain
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 582 · see citing works
Social brain development and the affective consequences of ostracism in adolescence
Sebastian, C., Viding, E., Williams, K. D., & Blakemore, S.-J. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.008 · Cited by 497 · see citing works
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · see citing works
“age range are most prominent in the frontal and parietal lobes.(8,58,59) Indeed, a recent study indicates that there is a progression in which higher cortical association areas like the PFC are last to show reduction of gray matter volume.”
BackgroundRubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007) · Human Brain Mapping · doi:10.1002/hbm.20347 · Cited by 417 · see citing works
Anatomical MRI of the developing human brain: what have we learned?
DURSTON, S., HULSHOFF POL, H. E., CASEY, B. J., GIEDD, J. N., BUITELAAR, J. K., & VAN ENGELAND, H. (2001) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200109000-00009 · Cited by 410 · see citing works
Brain maturation in adolescence: concurrent changes in neuroanatomy and neurophysiology
Whitford, T. J., Rennie, C. J., Grieve, S. M., Clark, C. R., Gordon, E., & Williams, L. M. (2007) · Human Brain Mapping · doi:10.1002/hbm.20273 · Cited by 391 · see citing works
SOWELL, E. R., DELIS, D., STILES, J., & JERNIGAN, T. L. (2001) · Journal of the International Neuropsychological Society · doi:10.1017/s135561770173305x · Cited by 388 · see citing works
Self-citationBurnett, S., Sebastian, C., Cohen Kadosh, K., & Blakemore, S.-J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.011 · Cited by 391 · see citing works
Durston, S., Pol, H. E. H., Schnack, H. G., Buitelaar, J. K., Steenhuis, M. P., Minderaa, R. B., Kahn, R. S., & van engeland, H. (2004) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200403000-00016 · Cited by 376 · see citing works
Ernst, M., & Fudge, J. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.009 · Cited by 358 · see citing works
Sonuga-Barke, E. J. S., Sergeant, J. A., Nigg, J., & Willcutt, E. (2008) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2007.11.008 · Cited by 348 · see citing works
Brain imaging of attention deficit/hyperactivity disorder
GIEDD, J. N., BLUMENTHAL, J., MOLLOY, E., & CASTELLANOS, F. X. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05772.x · Cited by 331 · see citing works
Age-related Volumetric Changes of Brain Gray and White Matter in Healthy Infants and Children
Matsuzawa, J. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.4.335 · Cited by 315 · see citing works
Mechanisms of postnatal neurobiological development: Implications for human development
Webb, S. J., Monk, C. S., & Nelson, C. A. (2001) · Developmental Neuropsychology · doi:10.1207/s15326942dn1902_2 · Cited by 272 · see citing works
Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain
Alfonso-Loeches, S., & Guerri, C. (2011) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2011.580567 · Cited by 254 · see citing works
Adolescent development of the neural circuitry for thinking about intentions
Blakemore, S.-J., den Ouden, H., Choudhury, S., & Frith, C. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm009 · Cited by 250 · see citing works
Memory Maintenance and Inhibitory Control Differentiate from Early Childhood to Adolescence
Shing, Y. L., Lindenberger, U., Diamond, A., Li, S.-C., & Davidson, M. C. (2010) · Developmental Neuropsychology · doi:10.1080/87565641.2010.508546 · Cited by 239 · see citing works
The maturation of incentive processing and cognitive control
Geier, C., & Luna, B. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.021 · Cited by 225 · see citing works
Sowell, E. R. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.17 · Cited by 212 · see citing works
Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry
Nugent, A. C., Milham, M. P., Bain, E. E., Mah, L., Cannon, D. M., Marrett, S., Zarate, C. A., Pine, D. S., Price, J. L., & Drevets, W. C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.029 · Cited by 206 · see citing works
Levine, B. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00280-x · Cited by 189 · see citing works
The Impact of Exposure to Cannabinoids in Adolescence: Insights From Animal Models
Rubino, T., & Parolaro, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.024 · Cited by 183 · see citing works
Feldstein Ewing, S. W., Sakhardande, A., & Blakemore, S.-J. (2014) · NeuroImage: Clinical · doi:10.1016/j.nicl.2014.06.011 · Cited by 185 · see citing works
Development of the Social Brain during Adolescence
Blakemore, S.-J. (2008) · Quarterly Journal of Experimental Psychology · doi:10.1080/17470210701508715 · Cited by 184 · see citing works
Do cognitive changes accompany developments in the adolescent brain?
Kuhn, D. (2006) · Perspectives on Psychological Science · doi:10.1111/j.1745-6924.2006.t01-2-.x · Cited by 161 · see citing works
Microbiota influence the development of the brain and behaviors in C57BL/6J mice
Lu, J., Synowiec, S., Lu, L., Yu, Y., Bretherick, T., Takada, S., Yarnykh, V., Caplan, J., Caplan, M., Claud, E. C., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201829 · Cited by 159 · see citing works
Rubia, K., Lim, L., Ecker, C., Halari, R., Giampietro, V., Simmons, A., Brammer, M., & Smith, A. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.078 · Cited by 133 · see citing works
The Development of Adolescent Social Cognition
Burnett, S., & Blakemore, S. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04509.x · Cited by 108 · see citing works
Lim, L., Marquand, A., Cubillo, A. A., Smith, A. B., Chantiluke, K., Simmons, A., Mehta, M., & Rubia, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063660 · Cited by 101 · see citing works
Social attitudes differentially modulate imitation in adolescents and adults
Cook, J., & Bird, G. (2011) · Experimental Brain Research · doi:10.1007/s00221-011-2584-4 · Cited by 92 · see citing works
Mapping brain size and cortical gray matter changes in elderly depression
Ballmaier, M., Sowell, E. R., Thompson, P. M., Kumar, A., Narr, K. L., Lavretsky, H., Welcome, S. E., DeLuca, H., & Toga, A. W. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.09.004 · Cited by 91 · see citing works
Self-citationKoshibu, K., Levitt, P., & Ahrens, E. T. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.051 · Cited by 62 · see citing works
Bergstrom, H. C., McDonald, C. G., French, H. T., & Smith, R. F. (2008) · Synapse · doi:10.1002/syn.20467 · Cited by 60 · see citing works
McNamara, R. K., Jandacek, R., Tso, P., Blom, T. J., Welge, J. A., Strawn, J. R., Adler, C. M., Strakowski, S. M., & DelBello, M. P. (2016) · Early Intervention in Psychiatry · doi:10.1111/eip.12282 · Cited by 50 · see citing works
Prefrontal cortex: Typical and atypical development
Dennis, M. (2006) · The Frontal Lobes · doi:10.1017/cbo9780511545917.007 · Cited by 41 · see citing works
Jamieson, D., Shan, Z., Lagopoulos, J., & Hermens, D. F. (2021) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2021.101450 · Cited by 28 · see citing works
Media Violence Effects on Brain Development: What Neuroimaging Has Revealed and What Lies Ahead
Hummer, T. A. (2015) · American Behavioral Scientist · doi:10.1177/0002764215596553 · Cited by 17 · see citing works
Age-Related Changes in Frontal and Temporal Lobe Volumes in Men: A Magnetic Resonance Imaging Study
Bartzokis, G., Beckson, M., Lu, P. H., Nuechterlein, K. H., Edwards, N., & Mintz, J. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.5.461 · Cited by 14 · see citing works
- Authors
- Sowell, E. R., Thompson, P. M., Holmes, C. J., Batth, R., Jernigan, T. L., & Toga, A. W.
- Affiliations
- University of California, Los Angeles (US)
- University of California San Diego (US)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 1999-06
- Volume
- 9
- Issue
- 6
- Pages
- 587-597
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2063322218
- Cited by
- 554
- References
- 1
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 5 · 2023: 14 · 2022: 10 · 2021: 9 · 2020: 13 · 2019: 15 · 2018: 16 · 2017: 19 · 2016: 13 · 2015: 29 · 2014: 23 · 2013: 36 · 2012: 26
- FWCI
- 10.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (5r01hd023854-07, 1p01dc001289-01)
- National Institute of Mental Health
- National Institute on Deafness and Other Communication Disorders (P01 DC01289)
- National Institute of Neurological Disorders and Stroke (P50 NS 22343, P50NS022343)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01 HD 23854)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
- Keywords
- gray matter volume, childhood to adolescence, brain development, frontal cortex, parietal cortex, dorsal cortex, tissue segmentation, white matter, structural MRI, permutation tests, brain aging
- MeSH terms
- Adolescent, Aging, Brain, Child, Female, Humans, Image Processing, Computer-Assisted, Male, Reproducibility of Results, Models, Statistical
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review