Effects of uncertainty in head tissue conductivity and complexity on EEG forward modeling in neonates

Abstract

In this study, we investigated the impact of uncertainty in head tissue conductivities and inherent geometrical complexities including fontanels in neonates. Based on MR and CT coregistered images, we created a realistic neonatal head model consisting of scalp, skull, fontanels, cerebrospinal fluid (CSF), gray matter (GM), and white matter (WM). Using computer simulations, we investigated the effects of exclusion of CSF and fontanels, discrimination between GM and WM, and uncertainty in conductivity of neonatal head tissues on EEG forward modeling. We found that exclusion of CSF from the head model induced the strongest widespread effect on the EEG forward solution. Discrimination between GM and white matter also induced a strong widespread effect, but which was less intense than that of CSF exclusion. The results also showed that exclusion of the fontanels from the neonatal head model locally affected areas beneath the fontanels, but this effect was much less pronounced than those of exclusion of CSF and GM/WM discrimination. Changes in GM/WM conductivities by 25% with respect to reference values induced considerable effects in EEG forward solution, but this effect was more pronounced for GM conductivity. Similarly, changes in skull conductivity induced effects in the EEG forward modeling in areas covered by the cranial bones. The least intense effect on EEG was caused by changes in conductivity of the fontanels. Our findings clearly emphasize the impact of uncertainty in conductivity and deficiencies in head tissue compartments on modeling research and localization of brain electrical activity in neonates. Hum Brain Mapp 37:3604-3622, 2016. © 2016 Wiley Periodicals, Inc.

Keywords: electroencephalography; finite element method; fontanels; forward modeling; head model; neonates; tissue conductivity.

Figure 1

Coronal, sagittal, and axial planes of the segmented head including GM,WM, CSF, cranial bones, fontanels, and scalp (a), and their corresponding 3D reconstruction (b). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Distribution of dipolar sources with cortical surface normal direction. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Distance map computed between cortical sources and the inner skull surface in mm. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Montage illustrating the location of 63 electrodes distributed according to the international 10–10 electrode placement system (a). The electrodes were grouped according to the thirteen cortical regions of interest (b). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

Cumulative relative frequencies for lnMAG (a) and RDM (b). The horizontal lines indicate frequencies of 95%.

Figure 6

RDM and lnMAG boxplots reflecting regional effects of inaccuracies in conductivities of the various head compartments and the effects of head model structural deficiencies on EEG forward modeling. See Figure 3 and Table I for abbreviations. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 7

Effect of CSF exclusion. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT1 (brain, skull, and scalp, σbrain = 0.33 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelT2 (brain, CSF, skull, and scalp, σbrain = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 8

Effect of CSF exclusion. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT1 (brain, skull, and scalp, σbrain = 0.33 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelT2 (brain, CSF, skull, and scalp, σbrain = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 9

Effect of gray/white matter discrimination. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT2 (brain, CSF, skull, and scalp, σbrain = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelT3 (white matter, gray matter, CSF, skull, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m). The differences between the two models are highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 10

Effect of gray/white matter discrimination. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT2 (brain, CSF, skull, and scalp, σbrain = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelT3 (white matter, gray matter, CSF, skull, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m). The differences between the two models are highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 11

Effect of exclusion of fontanels and sutures. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT3 (white matter, gray matter, CSF, skull, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The differences between the two models are highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 12

Effect of exclusion of fontanels and sutures. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT3 (white matter, gray matter, CSF, skull, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σskull = 0.04 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The differences between the two models are highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 13

Effect of skull conductivity. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT4 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 14

Effect of skull conductivity. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT4 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 15

Effect of gray matter conductivity. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT6 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.41 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 16

Effect of white matter conductivity. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT8 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.17 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 17

Effect of gray matter and white matter conductivity. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT6 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.41 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m), ModelT8 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.17 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.05 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The differences between the three models are highlighted in bold. Plots (a‐b) and (c‐d) show differences between (ModelT6 and ModelR) and (ModelT8 and ModelR), respectively. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 18

Effect of fontanel conductivity. lnMAG (upper row) and RDM (lower row) cortical (left column) and spherical (right column) maps. RDM and lnMAG were computed between ModelT10 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.41 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.54 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 19

Effect of fontanel conductivity. The 2D heat maps show differences in signal magnitude (lnMAG) and signal topography (RDM) between ModelT10 (white matter, gray matter, CSF, cranial bones (CB), fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.41 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.54 S/m, σscalp = 0.43 S/m) and ModelR (white matter, gray matter, CSF, cranial bones, fontanels, and scalp, σWM = 0.14 S/m, σGM = 0.33 S/m, σCSF = 1.79 S/m, σCB = 0.04 S/m, σfontanel = 0.43 S/m, σscalp = 0.43 S/m). The difference between the two models is highlighted in bold. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]