Greater Utilization of Neural-Circuits Related to Executive Functions is Associated with Better Reading: A Longitudinal fMRI Study Using the Verb Generation Task

Abstract

Introduction: Reading is an acquired-developmental ability that relies on intact language and executive function skills. Verbal fluency tasks (such as verb generation) also engage language and executive function skills. Performance of such tasks matures with normal language development, and is independent of reading proficiency. In this longitudinal fMRI study, we aim to examine the association between maturation of neural-circuits supporting both executive functions and language (assessed using verb generation) with reading proficiency achieved in adolescence with a focus on left-lateralization typical for language proficiency.

Methods: Normalized fMRI data from the verb generation task was collected from 16 healthy children at ages 7, 11, and 17 years and was correlated with reading scores at 17 years of age. Lateralization indices were calculated in key language, reading, and executive function-related regions in all age groups.

Results: Typical development was associated with (i) increasingly left-lateralized patterns in language regions (ii) more profound left-lateralized activation for reading and executive function-related regions when correlating with reading scores, (iii) greater involvement of frontal and parietal regions (in older children), and of the anterior frontal cortex (in younger children).

Conclusion: We suggest that reading and verb generation share mutual neural-circuits during development with major reliance on regions related to executive functions and reading. The results are discussed in the context of the dual-networks architecture model.

Keywords: development; dual-networks model; executive functions; fMRI; reading; verb generation.

Figure 1

Composite fMRI activation maps for the verb generation (verb generation > finger tapping) in T1 children (N = 16). The contrast is significant at p < 0.001 (corrected), slice thickness is 5 mm for these contiguous slices. Slices range from z = 13 to 24 in the Talairach frame. Cluster size is 30 voxels. Higher significance is indicated in hotter color (t threshold ranged from 3 to 6, see scale in the bottom of the figure). Figure is presented in a radiological orientation (L = R, R = L).

Figure 2

Composite fMRI activation maps for the verb generation (verb generation > finger tapping) in T2 children (N = 16). The contrast is significant at p < 0.001 (corrected), slice thickness is 5 mm for these contiguous slices. Slices range from z = 13 to 24 in the Talairach frame. Cluster size is 30 voxels. Higher significance is indicated in hotter color (t threshold ranged from 3 to 6). Figure is presented in a radiological orientation (L = R, R = L).

Figure 3

Composite fMRI activation maps for the verb generation (verb generation > finger tapping) in T3 children (N = 15). The contrast is significant at p < 0.001 (corrected), slice thickness is 5 mm for these contiguous slices. Slices range from z = 13 to 24 in the Talairach frame. Cluster size is 30 voxels. Higher significance is indicated in hotter color (t threshold ranged from 3 to 6). Figure is presented in a radiological orientation (L = R, R = L).

Figure 4

Regression maps showing a positive correlation for activation during verb generation scans in T1 with the Letter–Word score from the Woodcock–Johnson III (N = 16) in T3. All activated pixels meet significance threshold of p < 0.05, corrected. Slices range from z = 7 to 24 in the Talairach frame. Cluster size is 35 voxels. Higher significance is indicated in hotter color (r value ranged from 0.2 to 0.5, see scale in the bottom of the figure). Figure is presented in a radiological orientation (L = R, R = L).

Figure 5

Regression maps showing a positive correlation for activation during verb generation scans at T2 and the Letter–Word score from the Woodcock–Johnson III (N = 16) from T3. All activated pixels meet significance threshold of p < 001 uncorrected. Slices range from z = 7 to 24 in the Talairach frame. Cluster size is 35 voxels. Higher significance is indicated in hotter color (r value ranged from 0.2 to 0.5). Figure is presented in a radiological orientation (L = R, R = L).

Figure 6

Regression maps showing a positive correlation for activation during verb generation scans from T3 and the Letter–Word score from the Woodcock–Johnson III (N = 15) at T3. The activated pixels meet significance at p < 0.001, uncorrected, higher significance is indicated by hotter color. Slices range from z = 7 to 24 in the Talairach frame. Cluster size is 35 voxels. Higher significance is indicated in hotter color (r value ranged from 0.2 to 0.5). Figure is presented in a radiological orientation (L = R, R = L).

Figure 7

Lateralization index (LI) for the composite (upper) and the regression maps (lower). LI was calculated on language-related regions (Broca and Wernicke) in the composite maps in T1–T3. LI was also calculated on language (Broca and Wernicke), executive functions (dorsolateral prefrontal cortex, anterior prefrontal cortex), and reading regions (fusiform gyrus). Standard deviations representing the distribution of individual LIs are indicated.