Impact of puberty on the evolution of cerebral perfusion during adolescence

Satterthwaite, Theodore D.; Shinohara, Russell T.; Wolf, Daniel H.; Hopson, Ryan; Elliott, Mark A.; Vandekar, Simon; Ruparel, Kosha; Calkins, Monica E.; Roalf, David R.; Gennatas, Efstathios D.; Jackson, Chad; Erus, Güray; Prabhakaran, Karthik; Davatzikos, Christos; Detre, John A.; Hákonarson, Hákon; Gur, Ruben C.; Gur, Raquel E.

doi:10.1073/pnas.1400178111

Cited by 176 publications

(209 citation statements)

References 76 publications

(97 reference statements)

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“…To date, however, only a handful of nuclear medicine studies (Chiron et al, 1992;Chugani, 1998;Takahashi et al, 1999;Wintermark et al, 2004) reported developmental changes in CBF, CMRglu and CMRO 2 , suggesting a general peak around 5-8 years followed by tapering to adult levels throughout adolescence. Similar developmental trajectories of resting CBF have recently been shown by ASL perfusion MRI studies (Avants et al, 2015;Biagi et al, 2007;Satterthwaite et al, 2014;Taki et al, 2011aTaki et al, , 2011bWang and Licht, 2006;Wang et al, 2003). Detailed region and sex specific developmental trajectories of CBF have been revealed after the effect of age-related variations in cortical structure was adjusted (Satterthwaite et al, 2014;Taki et al, 2011aTaki et al, , 2011b.…”

Section: Developmental Trajectories Of Cbf and Cmro 2 At Baselinesupporting

confidence: 75%

“…Similar developmental trajectories of resting CBF have recently been shown by ASL perfusion MRI studies (Avants et al, 2015;Biagi et al, 2007;Satterthwaite et al, 2014;Taki et al, 2011aTaki et al, , 2011bWang and Licht, 2006;Wang et al, 2003). Detailed region and sex specific developmental trajectories of CBF have been revealed after the effect of age-related variations in cortical structure was adjusted (Satterthwaite et al, 2014;Taki et al, 2011aTaki et al, , 2011b. These studies suggest that ASL CBF may provide a valuable imaging marker of both typical and atypical development of brain function (Wang et al, 2009).…”

Section: Developmental Trajectories Of Cbf and Cmro 2 At Baselinesupporting

confidence: 72%

“…It has been shown that CBF is more closely related to neuronal activities through neurovascular coupling compared to BOLD signals (Chen et al, 2015). With careful adjustment of age related changes in gray matter volume and physiological parameters (Jain et al, 2012), region and sexspecific growth curves of CBF that diverge between the two sexes around puberty (Satterthwaite et al, 2014) have been observed. However, relating developmental CBF findings to the maturation of neuronal function may still be confounded by nonspecific vascular effects and subject to the strength of neurovascular coupling across developing populations (Leithner and Royl, 2014).…”

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confidence: 99%

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Developmental trajectories of cerebral blood flow and oxidative metabolism at baseline and during working memory tasks

et al. 2016

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The neurobiological interpretation of developmental BOLD fMRI findings remains difficult due to the confounding issues of potentially varied baseline of brain function and varied strength of neurovascular coupling across age groups. The central theme of the present research is to study the development of brain function and neuronal activity through in vivo assessments of cerebral blood flow (CBF), oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen (CMRO 2 ) both at baseline and during the performance of a working memory task in a cohort of typically developing children aged 7 to 18 years. Using a suite of 4 emerging MRI technologies including MR blood oximetry, phase-contrast MRI, pseudo-continuous arterial spin labeling (pCASL) perfusion MRI and concurrent CBF/BOLD fMRI, we found: 1) At baseline, both global CBF and CMRO 2 showed an age related decline while global OEF was stable across the age group; 2) During the working memory task, neither BOLD nor CBF responses showed significant variations with age in the activated fronto-parietal brain regions. Nevertheless, detailed voxel-wise analyses revealed sub-regions within the activated fronto-parietal regions that show significant decline of fractional CMRO 2 responses with age. These findings suggest that the brain may become more "energy efficient" with age during development.

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Section: Developmental Trajectories Of Cbf and Cmro 2 At Baselinesupporting

confidence: 75%

Section: Developmental Trajectories Of Cbf and Cmro 2 At Baselinesupporting

confidence: 72%

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confidence: 99%

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Developmental trajectories of cerebral blood flow and oxidative metabolism at baseline and during working memory tasks

et al. 2016

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“…Consistent with these findings, we have performed a comprehensive analysis on the structural connectome to elucidate sex differences in terms of individual connections [17], revealing stronger intrahemispheric connectivity (within both hemispheres) in males and stronger inter-hemispheric connectivity in females. The developmental course of sex differences is a less explored domain [11], mostly due to lack of large datasets spanning age ranges that include the developmental period, with a few exceptions in the case of structural, functional and behavioural modalities [11,16,17,21,32].…”

Section: Introductionmentioning

confidence: 99%

Establishing a link between sex-related differences in the structural connectome and behaviour

Tunç

Solmaz

Parker

et al. 2016

Phil. Trans. R. Soc. B

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133

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One contribution of 16 to a theme issue 'Multifaceted origins of sex differences in the brain'. Recent years have witnessed an increased attention to studies of sex differences, partly because such differences offer important considerations for personalized medicine. While the presence of sex differences in human behaviour is well documented, our knowledge of their anatomical foundations in the brain is still relatively limited. As a natural gateway to fathom the human mind and behaviour, studies concentrating on the human brain network constitute an important segment of the research effort to investigate sex differences. Using a large sample of healthy young individuals, each assessed with diffusion MRI and a computerized neurocognitive battery, we conducted a comprehensive set of experiments examining sex-related differences in the meso-scale structures of the human connectome and elucidated how these differences may relate to sex differences at the level of behaviour. Our results suggest that behavioural sex differences, which indicate complementarity of males and females, are accompanied by related differences in brain structure across development. When using subnetworks that are defined over functional and behavioural domains, we observed increased structural connectivity related to the motor, sensory and executive function subnetworks in males. In females, subnetworks associated with social motivation, attention and memory tasks had higher connectivity. Males showed higher modularity compared to females, with females having higher inter-modular connectivity. Applying multivariate analysis, we showed an increasing separation between males and females in the course of development, not only in behavioural patterns but also in brain structure. We also showed that these behavioural and structural patterns correlate with each other, establishing a reliable link between brain and behaviour. BackgroundWhile the presence of sex differences in human behaviour and cognition is well documented [1,2], our knowledge of anatomical foundations for such sex differences, specifically in the brain, is still relatively limited. The enigmatic interplay between brain and behaviour, and its modulation by sex, has intrigued scientists, philosophers and the general public for decades. Behavioural differences include, but are not limited to, enhanced motor [3,4] and spatial skills [5,6] in males and improved memory [7,8] and social cognition [9,10] skills in females [11]. These differences may be attributed to the complementary roles that the sexes play in procreation and social structure; however, increasing evidence suggests the presence of corresponding sex differences in brain structure and function [12][13][14][15][16][17], as well as the presence of a strong connection between behaviour and brain structure [12,18]. Thus, relying merely on social and cultural effects to explain sex-induced variance in behaviour seems insufficient. Notably, although sex differences in the brain are present even in childhood [16,17], the

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“…In support of this concept, there is growing evidence that in humans and experimental animals, the origins of pathologies associated with structural weakening of the vascular wall (e.g., intracerebral hemorrhages) occur during puberty, a time of rapid changes in the cerebral circulation and structural brain development (Blakemore et al 2010;Blanton et al 2012;Giedd et al 2006;Goddings et al 2014;Manz et al 1979;Peper et al 2011;Satterthwaite et al 2014). …”

Section: Discussionmentioning

confidence: 99%

IGF-1 deficiency in a critical period early in life influences the vascular aging phenotype in mice by altering miRNA-mediated post-transcriptional gene regulation: implications for the developmental origins of health and disease hypothesis

Tarantini

Giles

Wren

et al. 2016

AGE

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Epidemiological findings support the concept of Developmental Origins of Health and Disease, suggesting that early-life hormonal influences during a sensitive period of development have a fundamental impact on vascular health later in life. The endocrine changes that occur during development are highly conserved across mammalian species and include dramatic increases in circulating IGF-1 levels during adolescence. The present study was designed to characterize the effect of developmental IGF-1 deficiency on the vascular aging phenotype. To achieve that goal, early-onset endocrine IGF-1 deficiency was induced in mice by knockdown of IGF-1 in the liver using Cre-lox technology (Igf1 f/f mice crossed with mice expressing albumindriven Cre recombinase). This model exhibits lowcirculating IGF-1 levels during the peripubertal phase of development, which is critical for the biology of aging. Due to the emergence of miRNAs as important regulators of the vascular aging phenotype, the effect of early-life IGF-1 deficiency on miRNA expression profile in the aorta was examined in animals at 27 months of age. We found that developmental IGF-1 deficiency elicits persisting late-life changes in miRNA expression in the vasculature, which significantly differed from AGE (2016) 38:239-258

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Impact of puberty on the evolution of cerebral perfusion during adolescence

Cited by 176 publications

References 76 publications

Developmental trajectories of cerebral blood flow and oxidative metabolism at baseline and during working memory tasks

Developmental trajectories of cerebral blood flow and oxidative metabolism at baseline and during working memory tasks

Establishing a link between sex-related differences in the structural connectome and behaviour

IGF-1 deficiency in a critical period early in life influences the vascular aging phenotype in mice by altering miRNA-mediated post-transcriptional gene regulation: implications for the developmental origins of health and disease hypothesis

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