Language development and brain reorganization in a child born without the left hemisphere

Abstract

We present a case of a 14-year-old girl born without the left hemisphere due to prenatal left internal carotid occlusion. We combined longitudinal language and cognitive assessments with functional and structural neuroimaging data to situate the case within age-matched, typically developing children. Despite having had a delay in getting language off the ground during the preschool years, our case performed within the normal range on a variety of standardized language tests, and exceptionally well on phonology and word reading, during the elementary and middle school years. Moreover, her spatial, number, and reasoning skills also fell in the average to above-average range based on assessments during these time periods. Functional MRI data revealed activation in right fronto-temporal areas when listening to short stories, resembling the bilateral activation patterns in age-matched typically developing children. Diffusion MRI data showed significantly larger dorsal white matter association tracts (the direct and anterior segments of the arcuate fasciculus) connecting areas active during language processing in her remaining right hemisphere, compared to either hemisphere in control children. We hypothesize that these changes in functional and structural brain organization are the result of compensatory brain plasticity, manifesting in unusually large right dorsal tracts, and exceptional performance in phonology, speech repetition, and decoding. More specifically, we posit that our case's large white matter connections might have played a compensatory role by providing fast and reliable transfer of information between cortical areas for language in the right hemisphere.

Keywords: Diffusion MRI; Functional MRI; Language development; Left hemisphere lesion; Plasticity.

Fig. 1 –

Coronal, axial and sagittal views of C1 and L1 from the T1-weighted imaging scan.

Fig. 2 –

Scores of case C1 (green dot), S1 (red dot), L1, L2, and L3 (blue dots) overlaid on a boxplot of TD controls’ scores on standardized language measures: (A) Vocabulary (CDI, PPVT), (B) Early syntax (Syntax comprehension), (C) Late syntax (CELF-Formulated Sentences) (D) Early reading comprehension (WJ Passage Comprehension), (E) Later reading comprehension (Gates–MacGinitie Comprehension), (F) Decoding words (WJ Letter-Word Identification), (G) Decoding nonwords (WJ Word Attack), (H) Phonology (CTOPP Elision), (I) Calculation (WJ Calculation), (J) Word Problems (WJ Applied Problems). Note that C1 exhibited below normal to normal range performance relative to controls on measures (A)–(E), but consistently performed higher than controls on measures (F)–(H). C1 – TD comparisons with significantly different performance are indicated with an asterisk.

Fig. 2 –

Scores of case C1 (green dot), S1 (red dot), L1, L2, and L3 (blue dots) overlaid on a boxplot of TD controls’ scores on standardized language measures: (A) Vocabulary (CDI, PPVT), (B) Early syntax (Syntax comprehension), (C) Late syntax (CELF-Formulated Sentences) (D) Early reading comprehension (WJ Passage Comprehension), (E) Later reading comprehension (Gates–MacGinitie Comprehension), (F) Decoding words (WJ Letter-Word Identification), (G) Decoding nonwords (WJ Word Attack), (H) Phonology (CTOPP Elision), (I) Calculation (WJ Calculation), (J) Word Problems (WJ Applied Problems). Note that C1 exhibited below normal to normal range performance relative to controls on measures (A)–(E), but consistently performed higher than controls on measures (F)–(H). C1 – TD comparisons with significantly different performance are indicated with an asterisk.

Fig. 3 –

(A) Group activation maps of the Spoken Story versus Baseline fMRI comparison in TD controls, C1, and L1 as estimated in standard MNI space; in this figure, warm colors indicate higher activation for Spoken Stories > Baseline and cold colors higher activation for Baseline > Spoken Stories. (B) Conjunction z-score maps of Spoken Story > Baseline comparisons in TD controls as estimated in each individual’s native space; in this figure, warm colors indicate a higher count number of TD control participants who showed activation when listening to stories and cold colors indicate a lower count number. C1’s and L1’s z-score maps in the right hemisphere are outlined in black and overlaid on the TD right and left hemisphere conjunction maps, respectively. All contrast maps in this figure are displayed on a standard inflated cortical surface (164 k mesh) and thresholded individually at voxel-wise p = .001, cluster-wise FWE = .05.

Fig. 4 –

Boxplots representing the mean and distribution of Global Efficiency as well as Efficiency in language network nodes in the TD group with C1 (green dot), L1 (blue dot) and S1 (red dot) overlaid. Significant differences between C1’s right and either hemisphere in TD controls are indicated with an asterisk. Error bars represent Standard Error of the Mean.

Fig. 5 –

Sagittal views of the right direct AF (magenta), right anterior AF (yellow), right IFOF (orange), right ILF (brown), and right UF (cyan) traced in C1, L1, S1, and a typical TD control participant (the participant closest to the group average) overlaid on their anatomical images in native space (panels on the left). Tract volume (percent of total hemispheric volume in voxels) in C1 (green dot), L1 (blue dot) and S1 (red dot), overlayed on a boxplot representing the mean and distribution of the tracts in each hemisphere in control participants (graphs on the right). Error bars represent Standard Error of the Mean.