The Developmental Trajectory of Brain-Scalp Distance from Birth through Childhood: Implications for Functional Neuroimaging

Measurements of human brain function in children are of increasing interest in cognitive neuroscience. Many techniques for brain mapping used in children, including functional near-infrared spectroscopy (fNIRS), electroencephalography (EEG), magnetoencephalography (MEG) and transcranial magnetic stimulation (TMS), use probes placed on or near the scalp. The distance between the scalp and the brain is a key variable for these techniques because optical, electrical and magnetic signals are attenuated by distance. However, little is known about how scalp-brain distance differs between different cortical regions in children or how it changes with development. We investigated scalp-brain distance in 71 children, from newborn to age 12 years, using structural T1-weighted MRI scans of the whole head. Three-dimensional reconstructions were created from the scalp surface to allow for accurate calculation of brain-scalp distance. Nine brain landmarks in different cortical regions were manually selected in each subject based on the published fNIRS literature. Significant effects were found for age, cortical region and hemisphere. Brain-scalp distances were lowest in young children, and increased with age to up to double the newborn distance. There were also dramatic differences between brain regions, with up to 50% differences between landmarks. In frontal and temporal regions, scalp-brain distances were significantly greater in the right hemisphere than in the left hemisphere. The largest contributors to developmental changes in brain-scalp distance were increases in the corticospinal fluid (CSF) and inner table of the cranium. These results have important implications for functional imaging studies of children: age and brain-region related differences in fNIRS signals could be due to the confounding factor of brain-scalp distance and not true differences in brain activity

The developmental trajectory of brain-scalp distance from birth through childhood: implications for functional neuroimaging.

Measurements of human brain function in children are of increasing interest in cognitive neuroscience. Many techniques for brain mapping used in children, including functional near-infrared spectroscopy (fNIRS), electroencephalography (EEG), magnetoencephalography (MEG) and transcranial magnetic stimulation (TMS), use probes placed on or near the scalp. The distance between the scalp and the brain is a key variable for these techniques because optical, electrical and magnetic signals are attenuated by distance. However, little is known about how scalp-brain distance differs between different cortical regions in children or how it changes with development. We investigated scalp-brain distance in 71 children, from newborn to age 12 years, using structural T1-weighted MRI scans of the whole head. Three-dimensional reconstructions were created from the scalp surface to allow for accurate calculation of brain-scalp distance. Nine brain landmarks in different cortical regions were manually selected in each subject based on the published fNIRS literature. Significant effects were found for age, cortical region and hemisphere. Brain-scalp distances were lowest in young children, and increased with age to up to double the newborn distance. There were also dramatic differences between brain regions, with up to 50% differences between landmarks. In frontal and temporal regions, scalp-brain distances were significantly greater in the right hemisphere than in the left hemisphere. The largest contributors to developmental changes in brain-scalp distance were increases in the corticospinal fluid (CSF) and inner table of the cranium. These results have important implications for functional imaging studies of children: age and brain-region related differences in fNIRS signals could be due to the confounding factor of brain-scalp distance and not true differences in brain activity

Mean values at each landmark.

<p>Numbers represent the mean (μ) brain-scalp distance at each landmark in mm (± SD).</p

Components of brain-scalp distance.

<p><b>A. Enlarged axial slice through a newborn infant brain (subject FT2009, age 2 days).</b> White shows scale bar. Red letters show manually selected landmarks. <i>L</i>: Frontal pole landmark (outer boundary of cerebral cortex). <i>A</i>: Inner boundary of cranial bone marrow. <i>B</i>: Outer boundary of cranial bone marrow. <i>C</i>: Inner boundary of cutis. <i>D</i>: Outer boundary of cutis. <b>B. Enlarged axial slice through a child brain (subject CBP, age 12 years).</b> White shows scale bar. Red letters show manually selected landmarks.</p

Growth charts for brain-scalp distance.

<p>A. Mean growth chart averaged across all brain landmarks. Black line indicates best-fit growth function <i>D</i> = a * t+b where <i>D</i> is brain-scalp distance in mm (y – axis) and t is age in months (x – axis). Each blue square shows average brain-scalp distance in one subject. Fit parameters are a = 0.021, b = 8.5, <i>r²</i> = 0.15, F_1,88 = 16, p = 0.0001. B. Growth chart for Heschl's gyrus. Axis labels are the same as (A). Green squares indicate brain-scalp distance for left Heschl's gyrus in each individual subject and best-fit line; red squares indicate right Heschl's gyrus and best-fit line. Left hemisphere fit parameters are a = 0.013, b = 7.2, <i>r²</i> = 0.08, F_1,82 = 7, p = 0.01. Right hemisphere fit parameters are a = 0.014, b = 8.7, <i>r²</i> = 0.06, F_1,84 = 5, p = 0.02. C. Brain-scalp distance across age for left and right inferior frontal gyrus <i>par triangularis</i>. Left hemisphere fit parameters are a = 0.021, b = 8.75, <i>r²</i> = 0.1, F_1,87 = 10, p = 0.002. Right hemisphere fit parameters are a = 0.018, b = 10.2, <i>r²</i> = 0.07, F_1,77 = 6, p = 0.02. D. Growth chart for frontal pole landmark. Fit parameters are a = 0.010, b = 10.4, <i>r²</i> = 0.08, F_1,52 = 4, p = 0.04. E. Growth chart for occipital pole landmark. Fit parameters are a = 0.038, b = 4.7, <i>r²</i> = 0.48, F_1,86 = 80, p = 10⁻¹³. F. Growth chart for left and right parieto-occipital sulcus landmarks. Left hemisphere fit parameters are a = 0.028, b = 9.1, <i>r²</i> = 0.09, F_1,86 = 9, p = 0.004. Right hemisphere fit parameters are a = 0.029, b = 9.3, <i>r²</i> = 0.09, F_1,88 = 9, p = 0.004. G. Growth chart for vertex landmark. Fit parameters are a = 0.024, b = 9.1, <i>r²</i> = 0.10, F_1,85 = 9, p = 0.003.</p

Selection of anatomical landmarks.

<p>A. Lateral view of pial surface of left hemisphere. Color scale indicates distance between brain and scalp. Black circles indicate location of anatomical landmarks (IFG, inferior frontal gyrus <i>par triangularis</i>). B. Location of Heschl's gyrus anatomical landmark shown on axial slice. Green symbol inside white circle indicates landmark. White arrow highlights location. Yellow curve shows reconstruction of scalp surface. C. Location of inferior frontal gyrus <i>par triangularis</i> landmark on axial slice. D. Location of frontal pole landmark on axial slice. E. Location of occipital pole landmark on axial slice. F. Location of parietal landmark (superior and posterior most portion of parieto-occipital sulcus) on sagittal slice. G. Location of vertex landmark on sagittal slice.</p