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Research Articles, Development/Plasticity/Repair

Longitudinal Development of Brain Iron Is Linked to Cognition in Youth

Bart Larsen, Josiane Bourque, Tyler M. Moore, Azeez Adebimpe, Monica E. Calkins, Mark A. Elliott, Ruben C. Gur, Raquel E. Gur, Paul J. Moberg, David R. Roalf, Kosha Ruparel, Bruce I. Turetsky, Simon N. Vandekar, Daniel H. Wolf, Russell T. Shinohara and Theodore D. Satterthwaite
Journal of Neuroscience 26 February 2020, 40 (9) 1810-1818; DOI: https://doi.org/10.1523/JNEUROSCI.2434-19.2020
Bart Larsen
1Department of Psychiatry, Perelman School of Medicine,
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Josiane Bourque
1Department of Psychiatry, Perelman School of Medicine,
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Tyler M. Moore
1Department of Psychiatry, Perelman School of Medicine,
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Azeez Adebimpe
1Department of Psychiatry, Perelman School of Medicine,
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Monica E. Calkins
1Department of Psychiatry, Perelman School of Medicine,
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Mark A. Elliott
1Department of Psychiatry, Perelman School of Medicine,
2Department of Radiology,
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Ruben C. Gur
1Department of Psychiatry, Perelman School of Medicine,
2Department of Radiology,
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Raquel E. Gur
1Department of Psychiatry, Perelman School of Medicine,
2Department of Radiology,
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Paul J. Moberg
1Department of Psychiatry, Perelman School of Medicine,
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David R. Roalf
1Department of Psychiatry, Perelman School of Medicine,
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Kosha Ruparel
1Department of Psychiatry, Perelman School of Medicine,
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Bruce I. Turetsky
1Department of Psychiatry, Perelman School of Medicine,
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Simon N. Vandekar
5Department of Biostatistics, Vanderbilt University, Nashville, Tennessee 37235.
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Daniel H. Wolf
1Department of Psychiatry, Perelman School of Medicine,
3Center for Biomedical Image Computing and Analytics,
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Russell T. Shinohara
3Center for Biomedical Image Computing and Analytics,
4Department of Biostatistics, Epidemiology and Informatics, Pennsylvania Statistics in Imaging and Visualization Center, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and
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Theodore D. Satterthwaite
1Department of Psychiatry, Perelman School of Medicine,
3Center for Biomedical Image Computing and Analytics,
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Abstract

Brain iron is vital to multiple aspects of brain function, including oxidative metabolism, myelination, and neurotransmitter synthesis. Atypical iron concentration in the basal ganglia is associated with neurodegenerative disorders in aging and cognitive deficits. However, the normative development of brain iron concentration in adolescence and its relationship to cognition are less well understood. Here, we address this gap in a longitudinal sample of 922 humans aged 8–26 years at the first visit (M = 15.1, SD = 3.72; 336 males, 486 females) with up to four multiecho T2* scans each. Using this sample of 1236 imaging sessions, we assessed the longitudinal developmental trajectories of tissue iron in the basal ganglia. We quantified tissue iron concentration using R2* relaxometry within four basal ganglia regions, including the caudate, putamen, nucleus accumbens, and globus pallidus. The longitudinal development of R2* was modeled using generalized additive mixed models (GAMMs) with splines to capture linear and nonlinear developmental processes. We observed significant increases in R2* across all regions, with the greatest and most prolonged increases occurring in the globus pallidus and putamen. Further, we found that the developmental trajectory of R2* in the putamen is significantly related to individual differences in cognitive ability, such that greater cognitive ability is increasingly associated with greater iron concentration through late adolescence and young-adulthood. Together, our results suggest a prolonged period of basal ganglia iron enrichment that extends into the mid-twenties, with diminished iron concentration associated with poorer cognitive ability during late adolescence.

SIGNIFICANCE STATEMENT Brain tissue iron is essential to healthy brain function. Atypical basal ganglia tissue iron levels have been linked to impaired cognition in iron deficient children and adults with neurodegenerative disorders. However, the normative developmental trajectory of basal ganglia iron concentration during adolescence and its association with cognition are less well understood. In the largest study of tissue iron development yet reported, we characterize the developmental trajectory of tissue iron concentration across the basal ganglia during adolescence and provide evidence that diminished iron content is associated with poorer cognitive performance even in healthy youth. These results highlight the transition from adolescence to adulthood as a period of dynamic maturation of tissue iron concentration in the basal ganglia.

  • adolescence
  • basal ganglia
  • cognition
  • development
  • iron
  • R2*
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The Journal of Neuroscience: 40 (9)
Journal of Neuroscience
Vol. 40, Issue 9
26 Feb 2020
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Longitudinal Development of Brain Iron Is Linked to Cognition in Youth
Bart Larsen, Josiane Bourque, Tyler M. Moore, Azeez Adebimpe, Monica E. Calkins, Mark A. Elliott, Ruben C. Gur, Raquel E. Gur, Paul J. Moberg, David R. Roalf, Kosha Ruparel, Bruce I. Turetsky, Simon N. Vandekar, Daniel H. Wolf, Russell T. Shinohara, Theodore D. Satterthwaite
Journal of Neuroscience 26 February 2020, 40 (9) 1810-1818; DOI: 10.1523/JNEUROSCI.2434-19.2020

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Longitudinal Development of Brain Iron Is Linked to Cognition in Youth
Bart Larsen, Josiane Bourque, Tyler M. Moore, Azeez Adebimpe, Monica E. Calkins, Mark A. Elliott, Ruben C. Gur, Raquel E. Gur, Paul J. Moberg, David R. Roalf, Kosha Ruparel, Bruce I. Turetsky, Simon N. Vandekar, Daniel H. Wolf, Russell T. Shinohara, Theodore D. Satterthwaite
Journal of Neuroscience 26 February 2020, 40 (9) 1810-1818; DOI: 10.1523/JNEUROSCI.2434-19.2020
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Keywords

  • adolescence
  • basal ganglia
  • cognition
  • development
  • iron
  • R2*

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