Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood

Vincent J. Schmithorst, Jennifer Vannest, Gregory Lee, Luis Hernandez-Garcia, Elena Plante, Akila Rajagopal, Scott K. Holland

Research output: Contribution to journalArticle

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Abstract

Functional MRI using blood-oxygen-level-dependent (BOLD) imaging has provided unprecedented insights into the maturation of the human brain. Task-based fMRI studies have shown BOLD signal increases with age during development (ages 5-18) for many cognitive domains such as language and executive function, while functional connectivity (resting-state) fMRI studies investigating regionally synchronous BOLD fluctuations have revealed a developing functional organization of the brain from a local into a more distributed architecture. However, interpretation of these results is confounded by the fact that the BOLD signal is directly related to blood oxygenation driven by changes in blood flow and only indirectly related to neuronal activity, and may thus be affected by changing neuronal-vascular coupling. BOLD signal and cerebral blood flow (CBF) were measured simultaneously in a cohort of 113 typically developing awake participants ages 3-18 performing a narrative comprehension task. Using a novel voxelwise wild bootstrap analysis technique, an increased ratio of BOLD signal to relative CBF signal change with age (indicative of increased neuronal-vascular coupling) was seen in the middle temporal gyri and the left inferior frontal gyrus. Additionally, evidence of decreased relative oxygen metabolism (indicative of decreased neuronal activity) with age was found in the same regions. These findings raise concern that results of developmental BOLD studies cannot be unambiguously attributed to neuronal activity. Astrocytes and astrocytic processes may significantly affect the maturing functional architecture of the brain, consistent with recent research demonstrating a key role for astrocytes in mediating increased CBF following neuronal activity and for astrocyte processes in modulating synaptic connectivity. Hum Brain Mapp, 36:1-15, 2015.

Original languageEnglish (US)
Pages (from-to)1-15
Number of pages15
JournalHuman Brain Mapping
Volume36
Issue number1
DOIs
StatePublished - Jan 1 2015

Fingerprint

Oxygen
Brain
Astrocytes
Magnetic Resonance Imaging
Blood Vessels
Executive Function
Temporal Lobe
Prefrontal Cortex

Keywords

  • Children
  • Developmental studies
  • Functional MRI
  • Language processing
  • Neuronal-vascular coupling

ASJC Scopus subject areas

  • Clinical Neurology
  • Anatomy
  • Neurology
  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology

Cite this

Schmithorst, V. J., Vannest, J., Lee, G., Hernandez-Garcia, L., Plante, E., Rajagopal, A., & Holland, S. K. (2015). Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood. Human Brain Mapping, 36(1), 1-15. DOI: 10.1002/hbm.22608

Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood. / Schmithorst, Vincent J.; Vannest, Jennifer; Lee, Gregory; Hernandez-Garcia, Luis; Plante, Elena; Rajagopal, Akila; Holland, Scott K.

In: Human Brain Mapping, Vol. 36, No. 1, 01.01.2015, p. 1-15.

Research output: Contribution to journalArticle

Schmithorst, VJ, Vannest, J, Lee, G, Hernandez-Garcia, L, Plante, E, Rajagopal, A & Holland, SK 2015, 'Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood' Human Brain Mapping, vol 36, no. 1, pp. 1-15. DOI: 10.1002/hbm.22608
Schmithorst VJ, Vannest J, Lee G, Hernandez-Garcia L, Plante E, Rajagopal A et al. Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood. Human Brain Mapping. 2015 Jan 1;36(1):1-15. Available from, DOI: 10.1002/hbm.22608

Schmithorst, Vincent J.; Vannest, Jennifer; Lee, Gregory; Hernandez-Garcia, Luis; Plante, Elena; Rajagopal, Akila; Holland, Scott K. / Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood.

In: Human Brain Mapping, Vol. 36, No. 1, 01.01.2015, p. 1-15.

Research output: Contribution to journalArticle

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