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Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network.
Abstract
The aim of this study was to explore whether there are networks of regions where maturation of white matter and changes in brain activity show similar developmental trends during childhood. In a previous study, we showed that during childhood, grey matter activity increases in frontal and parietal regions. We hypothesized that this would be mediated by maturation of white matter. Twenty-three healthy children aged 8-18 years were investigated. Brain activity was measured using the blood oxygen level-dependent (BOLD) contrast with functional magnetic resonance imaging (fMRI) during performance of a working memory (WM) task. White matter microstructure was investigated using diffusion tensor imaging (DTI). Based on the DTI data, we calculated fractional anisotropy (FA), an indicator of myelination and axon thickness. Prior to scanning, WM score was evaluated. WM score correlated independently with FA values and BOLD response in several regions. FA values and BOLD response were extracted for each subject from the peak voxels of these regions. The FA values were used as covariates in an additional BOLD analysis to find brain regions where FA values and BOLD response correlated. Conversely, the BOLD response values were used as covariates in an additional FA analysis. In several cortical and sub-cortical regions, there were positive correlations between maturation of white matter and increased brain activity. Specifically, and consistent with our hypothesis, we found that FA values in fronto-parietal white matter correlated with BOLD response in closely located grey matter in the superior frontal sulcus and inferior parietal lobe, areas that could form a functional network underlying working memory function.
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“Analytical methods using a combination of DTI and fMRI have also demonstrated a positive correlation between the maturation of prefrontal-parietal connectivity and performance on working memory tasks (Olesen et al. 2003).”
From Developmental Changes in Organization of Structural Brain Networks (2013) · cites this paper as Olesen et al. 2003
In the citing paper
“Furthermore, in the same group of children, the variability in FA in the left fronto-parietal cluster that exhibited a relationship to SWM performance was also positively correlated with SWM-related fMRI activity in the left inferior parietal lobe and left superior frontal sulcus (Olesen, Nagy, Westerberg, & Klingberg, 2003).”
From White Matter Microstructure in Superior Longitudinal Fasciculus Associated with Spatial Working Memory Performance in Children (2011) · cites this paper as Olesen et al., 2003
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White matter microstructure is associated with cognitive control in children
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“Frontoparietal white matter maturation correlates with an increase in grey matter activity in both lobes during performance of a working memory (WM) task indicating the close functional connection [10].”
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“Moreover, these FA values were positively correlated with the BOLD response in superior frontal sulcus and intraparietal cortex (Olesen et al. 2003).”
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“To this aim we applied PAS over the DLPFC and the PPC, given the crucial role of the connections between these two areas in largescale memory and attention processes (Olesen et al., 2003; 2004; Sauseng et al., 2005).”
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“Even in normal patients, DTI imaging shows a significant correlation between working memory function and maturation of white matter tract connectivity between the PFC and the parietal lobe.(92) PFC and IPL have reciprocal connections with the cerebellum with input passing through the internal capsule and pons and outp…”
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InfluentialNeural correlates of the development of cognitive control
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“Moreover, a comparison of fMRI data and diffusion tensor imaging data reveals that increased fractional anisotropy in fronto-parietal white matter – suggestive of increased strength of anatomical connectivity between these regions – is positively correlated with blood-oxygen-level-dependent (BOLD) activation in the SF…”
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“…studies have linked increasing myelination of major white matter tracts across adolescence (Barnea-Goraly et al., 2005; Schmithorst et al., 2008) to both brain activation maturation and cognitive test performance (Nagy et al., 2004; Olesen et al., 2003), ch Center, Whitehall Building, 06106, USA.”
BackgroundDevelopmental shifts in fMRI activations during visuospatial relational reasoning
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“Similarly, developmental imaging of visuospatial working memory has shown that both age and working memory ability are positively correlated with activation in parietal and superior frontal cortices (Klingberg, Forssberg, & Westerberg, 2002; Kwon, Reiss, & Menon, 2002) as well as maturation of white matter tracts link…”
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“Finally, it has been reported that FA values in frontoparietal white matter correlate strongly with BOLD response (during a working memory task) in closely located gray matter in the superior frontal sulcus and inferior parietal lobe ( Oleson, Nagy, Westerberg, & Klingberg, 2003 ).”
BackgroundMultiple Concurrent Thoughts: The Meaning and Developmental Neuropsychology of Working Memory
Cowan, N. (2010) · Developmental Neuropsychology · doi:10.1080/87565641.2010.494985 · Cited by 79
A Multimodal Assessment of the Genetic Control over Working Memory
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InfluentialDistinct neural substrates for deductive and mathematical processing
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BackgroundA Selective Review of Multimodal Fusion Methods in Schizophrenia
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“There have been several studies investigating age-related changes of white matter and the corresponding changes in cognitive measures (e.g., Olesen et al., 2003; Nagy et al., 2004; Zahr et al., 2009; Bava, et al., 2010).”
BackgroundSpecial considerations for functional magnetic resonance imaging of pediatric populations
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“This methodology may allow us to determine if developmental changes in separate regions of activation are associated with simultaneous developmental changes in connectivity between those regions (70,71).”
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Mental imagery, emotion and psychopathology across child and adolescent development
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“Furthermore, normative developmental studies suggest that the dorsal pathway has a more protracted maturational trajectory than the ventral stream [66], and WM fMRI studies demonstrate greater parietal [4,73] but less fusiform recruitment [66] with age.”
BackgroundBlanken, L. M. E., White, T. J. H., Mous, S. E., Basten, M., Muetzel, R. L., Jaddoe, V. W. V., Wals, M., van der Ende, J., Verhulst, F. C., & Tiemeier, H. W. (2016) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-016-0903-9 · Cited by 76
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“children have identified significant correlations between visual WM performance and development of white matter in left frontoparietal regions, as well as in the anterior corpus callosum (CC).(31,32)”
BackgroundVerbal Memory Impairments in Children after Cerebellar Tumor Resection
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BackgroundResultInfluentialCOMT genotype affects prefrontal white matter pathways in children and adolescents
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“Higher FA and lower diffusivity are functionally significant (Deutsch et al., 2005; Dougherty et al., 2007; Olesen et al., 2003) and have been described as markers of developmental progress (Barnea-Goraly et al., 2005b; Eluvathingal et al., 2007; Lebel et al., 2008b; McGraw et al., 2002; Morriss et…”
Is activity regulation of late myelination a plastic mechanism in the human nervous system?
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“Correlations between maturation of white matter and increased brain activity during performance of a working memory task have been reported in a normative sample (Olesen et al., 2003).”
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BackgroundMyelination shapes functional activity in the developing brain
Fornari, E., Knyazeva, M. G., Meuli, R. A., & Maeder, P. P. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.010 · Cited by 66
“There exists another report pointing to the associated myelination of the long-range cortical connections and activation of their target areas in children aged 8–18 years (Olesen et al., 2003).”
BackgroundEmerging Structure-Function Relations in the Developing Face Processing System
Scherf, K. S., Thomas, C., Doyle, J., & Behrmann, M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht152 · Cited by 65
Attention Deficit Hyperactivity Disorder
Matthews, M., Nigg, J. T., & Fair, D. A. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_249 · Cited by 80
“network (Olesen et al. 2003), while better visuospatial construction and psychomotor performance is associated with high corpus callosum fractional anisotropy (Fryer et al.”
BackgroundBaldoli, C., Scola, E., Rosa, P. D. D., Pontesilli, S., Longaretti, R., Poloniato, A., Scotti, R., Blasi, V., Cirillo, S., Iadanza, A., et al. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0887-5 · Cited by 55
Structural correlates of impaired working memory in hippocampal sclerosis
Winston, G. P., Stretton, J., Sidhu, M. K., Symms, M. R., Thompson, P. J., & Duncan, J. S. (2013) · Epilepsia · doi:10.1111/epi.12193 · Cited by 59
“Maturation of the gray and white matter of the frontoparietal network is seen in healthy children (Olesen et al., 2003) and is related to working memory performance (Nagy et al., 2004; Ostby et al., 2011).”
BackgroundBeek, L. V., Ghesquière, P., Lagae, L. G., & Smedt, B. D. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.12.030 · Cited by 57
“…factors, such as crossing fibers, is commonly used and has been successful in identifying the neuro-anatomical correlates of cognitive functions, such as working memory (e.g., Olesen et al., 2003), intelligence (e.g., Schmithorst et al., 2005) and reading (Vandermosten et al., 2012b, for a review).”
BackgroundMethodScherder, E., Eggermont, L. H. P., Visscher, C., Scheltens, P., & Swaab, D. F. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.08.009 · Cited by 62
Tervo‐Clemmens, B., Simmonds, D. J., Calabro, F. J., Day, N. L., Richardson, G. A., & Luna, B. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.12.041 · Cited by 62
“Importantly, subcortical regions (Giedd et al., 1996) and lateral prefrontal (Ordaz et al., 2013) and posterior parietal cortices (PPC) (Olesen et al., 2003) undergo significant maturation during adolescence.”
BackgroundOn the working memory of humans and great apes: Strikingly similar or remarkably different?
Read, D., Manrique, H. M., & WALKER, M. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.019 · Cited by 58
Visual recovery after perinatal stroke evidenced by functional and diffusion MRI: case report
Seghier, M. L., Lazeyras, F., Zimine, S., Saudan-Frei, S., Safran, A. B., & Hüppi, P. S. (2005) · BMC Neurology · doi:10.1186/1471-2377-5-17 · Cited by 56
“The combination of both techniques (fMRI and DTI) has opened up the opportunity to investigate structure-function relationships non-invasively in children [6,7].”
BackgroundSeghier, M. L., Lazeyras, F., & Hüppi, P. S. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.007 · Cited by 57
Ekman, M., Fiebach, C. J., Melzer, C., Tittgemeyer, M., & Derrfuß, J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1376-14.2016 · Cited by 62
“Most previous studies that have investigated white matter contributions to individual WMC differences focused on local white matter integrity of individual regions (Olesen et al., 2003; Nagy et al., 2004).”
BackgroundD’Andrea, A., Chella, F., Marshall, T. R., Pizzella, V., Romani, G. L., Jensen, O. B., & Marzetti, L. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.12.056 · Cited by 55
“To this end, the ACB analysis was run by choosing as reference regions bilateral frontal areas, in proximity of the FEFs (Olesen et al., 2003; Marshall et al., 2015).”
InfluentialLi, M., Wang, Y., Tachibana, M., Rahman, M. S., & Kagitani‐Shimono, K. (2022) · Autism Research · doi:10.1002/aur.2789 · Cited by 64
“The development of gray matter activity seems to be mediated by the maturation of white matter (Olesen et al., 2003).”
BackgroundEvaluation of the GTRACT diffusion tensor tractography algorithm: A validation and reliability study
Cheng, P., Magnotta, V. A., Wu, D. H., Nopoulos, P., Moser, D. J., Paulsen, J. S., Jorge, R. E., & Andreasen, N. C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.01.028 · Cited by 54
Kim, Y., Jeong, K. S., Song, H., Lee, J., Seo, J., Kim, G.-C., Lee, H. J., Kim, H. J., Ahn, J., Park, S.-J., et al. (2010) · NeuroToxicology · doi:10.1016/j.neuro.2010.11.004 · Cited by 53
Neonatal MRI is associated with future cognition and academic achievement in preterm children
Ullman, H., Spencer‐Smith, M. M., Thompson, D. K., Doyle, L. W., Inder, T. E., Anderson, P. J., & Klingberg, T. (2015) · Brain · doi:10.1093/brain/awv244 · Cited by 58
Visuospatial working memory in very preterm and term born children—Impact of age and performance
Mürner-Lavanchy, I. M., Ritter, B. C., Spencer‐Smith, M. M., Perrig, W. J., Schroth, G., Steinlin, M. I., & Everts, R. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.02.004 · Cited by 56
“It is possible that the younger, low-performing very preterm born children cannot engage the same widespread network seen in controls, because they are still in the process of functional organization of working memory, leading to different network characteristics (Olesen et al., 2003).”
BackgroundAging: Compensation or maturation?
Aine, C. J., Woodruff, C. C., Knoefel, J. E., Adair, J. C., Hudson, D., Qualls, C., Bockholt, J. H., Best, E., Kovačević, S., Cobb, W., et al. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.05.005 · Cited by 53
“Olesen et al. (2003) combined data from DTI and fMRI from children (8–18 years) and showed positive correlations between WM maturation (FA measures) and neural activity (BOLD responses) in a number of regions important for spatial working memory and the development of working memory capacity (e.g.,…”
Default mode network scaffolds immature frontoparietal network in cognitive development
Chen, M., He, Y., Lei, H. C., Xu, J., Tian, T., Peng, S., Zhao, G., Lu, J., Zhao, Y., Zhao, H., et al. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac414 · Cited by 55
“Thus, findings from structural and functional MRI studies have demonstrated that the FPN regions undergo protracted development (Johnson 2001; Klingberg et al. 2002; Olesen et al. 2003; Alvarez and Emory 2006; Fair et al. 2007), with slower maturation than the DMN from childhood to adulthood (Supekar et al.”
BackgroundHernandez-Pavon, J. C., Agustín, A. S., Wang, M. C., Veniero, D., & Pons, J. L. (2023) · Clinical Neurophysiology · doi:10.1016/j.clinph.2023.06.016 · Cited by 51
“LDLPFC to LPPC Substantial evidence demonstrates that the connections between the dorsolateral prefrontal cortex (DLPFC) and PPC are relevant for memory, attentional processes, and choice (Essex et al., 2012; Olesen et al., 2003; Sauseng et al., 2005).”
Childhood cognitive development as a skill
Klingberg, T. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.06.007 · Cited by 60
Corpus callosum morphology and ventricular size in chromosome 22q11.2 deletion syndrome
Machado, A. M. C., Simon, T. J., Nguyen, V., McDonald‐McGinn, D. M., Zackai, E. H., & Gee, J. C. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.082 · Cited by 48
“…task that has been shown, at least in typically developing adults, to depend heavily on the posterior aspects of the frontoparietal attention network (Piazza et al., 2002; Sathian et al., 1999) was found to directly relate tomeasures of the anterior corpus callosum in children with DS22q11.”
BackgroundChechlacz, M., Rotshtein, P., & Humphreys, G. W. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.09.038 · Cited by 48
“…associated with both memory and language deficits in temporal lobe epilepsy and white matter maturation within the arcuate fasciculus including the temporoparietal segment is a predictor of visuospatial memory capacity in childhood (McDonald et al., 2008; Olesen et al., 2003; Short et al., 2013).”
Teslovich, T., Mulder, M., Franklin, N. T., Ruberry, E. J., Millner, A., Somerville, L. H., Simen, P., Durston, S., & Casey, B. J. (2014) · Developmental Science · doi:10.1111/desc.12092 · Cited by 45
“Continued development of this circuitry throughout adolescence (Fair et al., 2007; Klingberg et al., 2002; Olesen et al., 2003) may lead to differences in how incentives can modulate decisions in adolescents relative to adults (van den Bos et al.”
BackgroundZiermans, T. B., Dumontheil, I., Roggeman, C., Peyrard‐Janvid, M., Matsson, H., Kere, J., & Klingberg, T. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.7 · Cited by 48
Takeuchi, H., Taki, Y., Sassa, Y., Hashizume, H., Sekiguchi, A., Nagase, T., Nouchi, R., Fukushima, A., & Kawashima, R. (2011) · Human Brain Mapping · doi:10.1002/hbm.21492 · Cited by 50
“WM integrity, found in nonclinical samples is associated with cognitive function with reference to nonsocial and nonemotional thought processes [Jung et al., 2010a; Olesen et al., 2003; Schmithorst et al., 2005; Takeuchi et al., 2010d].”
BackgroundResultNeural correlates of working memory development in adolescent primates
Zhou, X., Zhu, D., Qi, X.-L., Li, S., King, S. G., Salinas, E., Stanford, T. R., & Constantinidis, C. (2016) · Nature Communications · doi:10.1038/ncomms13423 · Cited by 47
“Anatomical changes in the prefrontal cortex that continue throughout adolescence include increases in grey and white matter volumes, and in myelination of axon fibres within the prefrontal cortex and between the prefrontal cortex and other brain areas 6–13 .”
The U Sign: Tenth Landmark to the Central Region on Brain Surface Reformatted MR Imaging
Wagner, M., Jurcoane, A., & Hattingen, E. (2012) · American Journal of Neuroradiology · doi:10.3174/ajnr.a3205 · Cited by 45
Effects of traumatic brain injury on working memory-related brain activation in adolescents.
Newsome, M. R., Steinberg, J. L., Scheibel, R. S., Troyanskaya, M., Chu, Z. D., Hanten, G. R., Lu, H., Lane, S., Lin, X., Hunter, J. V., et al. (2008) · Neuropsychology · doi:10.1037/0894-4105.22.4.419 · Cited by 45
“Later studies of TD children reported fronto-parietal activation during visuospatial working memory tasks (Klingberg et al., 2002; Olesen et al., 2003; Thomas et al., 1999), with evidence for an age-related increase in working memory activation between 9 and 18 years (Klingberg et al., 2002).”
BackgroundPascoe, L., Roberts, G., Doyle, L. W., Lee, K. J., Thompson, D. K., Seal, M. L., Josev, E. K., Nosarti, C., Gathercole, S. E., & Anderson, P. J. (2013) · BMC Pediatrics · doi:10.1186/1471-2431-13-144 · Cited by 49
“Studies have illustrated that the maturation of white matter fibre tracts, such as the superior longitudinal fasciculus, positively correlate with the functional activation of frontal and parietal regions involved with working memory [48,59].”
Sundaram, S. K., Sivaswamy, L., Makki, M., Behen, M. E., & Chugani, H. T. (2007) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2007.06.037 · Cited by 44
Stufflebeam, S. M., Witzel, T., Mikulski, S., Hämäläinen, M., Temereanca, S., Barton, J. J. S., Tuch, D. S., & Manoach, D. S. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.264 · Cited by 44
“…as the amplitude of steady-state visual evoked potentials (Butler et al., 2005), measures of functional connectivity (Boorman et al., 2007), and task-related BOLD signal (Baird et al., 2005; Olesen et al., 2003), this is the first report of relations between FA and the timing of evoked responses.”
BackgroundDiffusion tensor imaging of hemispheric asymmetries in the developing brain
Wilde, E. A., McCauley, S. R., Chu, Z. D., Hunter, J. V., Bigler, E. D., Yallampalli, R., Wang, Z., Hanten, G. R., Li, X., Ramos, M. A., et al. (2008) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390802098118 · Cited by 43
“…verbal skills in girls than in boys and diffusivity decreasing with typical brain development (Bonekamp et al., 2007), we interpret low left relative to right temporal diffusivity as an indication of brain maturation in boys, a condition that may enhance reading comprehension (Olesen et al., 2003).”
Sudre, G. P., Frederick, J., Sharp, W. S., Ishii‐Takahashi, A., Mangalmurti, A., Choudhury, S., & Shaw, P. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0350-3 · Cited by 42
Schoonheim, M. M., Douw, L., Broeders, T. A. A., Eijlers, A. J. C., Meijer, K. A., & Geurts, J. J. G. (2021) · Multiple Sclerosis Journal · doi:10.1177/1352458521999274 · Cited by 42
Brain connectivity during verbal working memory in children and adolescents
van den Bosch, G. E., Marroun, H. E., Schmidt, M. N., Tibboel, D., Manoach, D. S., Calhoun, V. D., & White, T. J. H. (2012) · Human Brain Mapping · doi:10.1002/hbm.22193 · Cited by 46
“While children have been shown to activate similar brain regions as adults [Nelson et al., 2000; Olesen et al., 2003] there are several distinct developmental differences, although the findings are inconsistent.”
BackgroundIncreased integrity of white matter pathways after dual n-back training
Salminen, T., Mårtensson, J., Schubert, T., & Kühn, S. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.028 · Cited by 43
“WM processes are associated with the PFC, and in children and adolescents a higher FA in the genu of corpus callosum and in the temporo-occipital node is associated with a better WM performance (Nagy et al., 2004; Olesen et al., 2003).”
Individual Differences in White Matter Microstructure in the Healthy Brain
Scholz, J., Tomassini, V., & Johansen‐Berg, H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-396460-1.00014-7 · Cited by 45
Metadata
- Authors
- Olesen, P. J., Nagy, Z., Westerberg, H., & Klingberg, T.
- Affiliations
- Karolinska Institutet (SE)
- Corresponding author
- Olesen, Pernille J
- ORCID
- Klingberg, Torkel
- Venue
- Cognitive Brain Research
- Publisher
- Elsevier BV
- Published
- 2003-12
- Volume
- 18
- Issue
- 1
- Pages
- 48-57
- ISSN
- 0926-6410 (ISSN-L)
- OpenAlex
- W2132801576
- Cited by
- 397
- References
- 62
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 6 · 2023: 7 · 2022: 5 · 2021: 13 · 2020: 9 · 2019: 8 · 2018: 11 · 2017: 17 · 2016: 21 · 2015: 25 · 2014: 21 · 2013: 42 · 2012: 29
- FWCI
- 9.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cognitive Brain Research (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Vetenskapsrådet
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- brain maturation, white matter maturation, frontoparietal network, working memory, fractional anisotropy, myelination, BOLD signal, children, superior frontal sulcus, inferior parietal lobule, white matter microstructure
- MeSH terms
- Adolescent, Cerebral Cortex, Child, Female, Frontal Lobe, Humans, Magnetic Resonance Imaging, Male, Myelin Sheath, Nerve Net, Parietal Lobe, Diffusion Magnetic Resonance Imaging
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