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

Date Published: September 21, 2011

Publisher: Public Library of Science

Author(s): Michael S. Beauchamp, Michelle R. Beurlot, Eswen Fava, Audrey R. Nath, Nehal A. Parikh, Ziad S. Saad, Heather Bortfeld, John S. Oghalai, Evan Balaban.

Abstract: 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.

Partial Text: Human brain and behavior both undergo remarkable changes during development, and there is intense interest in using functional neuroimaging techniques to better understand neurodevelopment. Many of these techniques, including fNIRS, EEG, MEG and TMS measure (or evoke) brain function using probes placed on or near the scalp. The physical distance between the scalp and brain is therefore a critical parameter for these techniques, especially for fNIRS. In fNIRS, and in related techniques such as event-related optical signaling [1], low-power near-infrared light is directed through the scalp and intervening tissues into the surface of the brain [2], [3]. Due to the differential absorption of specific wavelengths of near-infrared light by oxygenated and deoxygenated hemoglobin, concentration changes can be determined by measuring changes in the amount of near-infrared light sensed by detectors located on the scalp some distance from the near-infrared transmitter. Hence, fNIRS measures the same hemodynamic signal as measured with blood-oxygen level dependent functional magnetic resonance imaging (BOLD fMRI), the most popular method for examining human brain function [4], [5]. However, unlike fMRI, fNIRS depends on the transmission of light through the scalp, skull, meninges and CSF. The spatial sensitivity profile of fNIRS can be characterized as having a “banana” shape, with one end of the banana at the emitter, one end at the detector, and the body of the banana dipping down to sample the cortex [6]. The optimal placement of the detector and emitter therefore depends on the depth that light must penetrate: if the emitter and detector are close, more light will travel from the emitter to the detector, but none will travel through the brain; if the emitter and detector are distant, little light will reach the detector, resulting in poor signal-to-noise ratio. Our study was spurred by our experience in recording responses from auditory cortex in children with fNIRS [7]. In order to determine the optimal emitter-detector distance, we wanted to establish the distance between the brain and scalp for the different aged children in our study population. While there are published studies of brain-scalp distance in adults [8], [9], [10] and children [11], [12], we could find little information on how brain-scalp distance changes during development. To fill this gap, we examined MRI scans from 71 healthy children ranging in age from 1 day to 12 years old. We hypothesized that there would be significant differences between ages, with younger children having reduced brain-scalp distances; and significant differences between brain areas, with greater brain-scalp distances in some regions relative to others.

Experiments were conducted in accordance with the Institutional Review Board of the University of Texas Health Science Center at Houston. Written informed consent was obtained from the guardian of each subject, and assent from the child subject if appropriate, prior to data collection. Information about scalp-brain distance was extracted from T1-weighted anatomical MRI images collected from each subject. The total subject population (n = 71) was assembled from 3 datasets.

Our examination of brain-scalp distance was motivated by the desire to use fNIRS to examine auditory and language function in patients that spanned a wide age range [7]. As fNIRS depends on the transmission of infrared photons through the skull and brain tissues, changes in brain-scalp distance present an additional confounding variable that is little understood. We found significant differences between brain regions, with the greatest brain-scalp distance over parietal regions, and the smallest difference over more inferior regions of the occipital and temporal lobes. There was a significant effect of laterality in some brain areas, with greater brain-scalp distance in right compared with left temporal and frontal regions. Across landmarks, brain-scalp distance increased with age, with the exception of the frontal pole, where it stayed relatively constant.