Differential development of the ventral visual cortex extends through adolescence

Abstract

The ventral temporal cortex (VTC) in humans includes functionally defined regions that preferentially respond to objects, faces, and places. Recent developmental studies suggest that the face selective region in the fusiform gyrus ('fusiform face area', FFA) undergoes a prolonged development involving substantial increases in its volume after 7 years of age. However, the endpoint of this development is not known. Here we used functional magnetic resonance imaging (fMRI) to examine the development of face-, object- and place selective regions in the VTC of adolescents (12-16 year olds) and adults (18-40 year olds). We found that the volume of face selective activations in the right fusiform gyrus was substantially larger in adults than in adolescents, and was positively correlated with age. This development was associated with higher response amplitudes and selectivity for faces in face selective regions of VTC and increased differentiation of the distributed response patterns to faces versus non-face stimuli across the entire VTC. Furthermore, right FFA size was positively correlated with face recognition memory performance, but not with recognition memory of objects or places. In contrast, the volume of object- and place selective cortical regions or their response amplitudes did not change across these age groups. Thus, we found a striking and prolonged development of face selectivity across the VTC during adolescence that was specifically associated with proficiency in face recognition memory. These findings have important implications for theories of development and functional specialization in VTC.

Keywords: adolescent; development; face processing; fusiform face area; gender; parahippocampal place area; ventral temporal cortex.

Figure 1

Behavioral data during scan. (A) Accuracy and (B) response times in a 1-back task during the scan. Light gray: adolescents ages 12–16 years; Black: adults ages 18–40 years. Error bars show standard error of mean (SEM) for each age group. Asterisk indicates significantly higher accuracy in adolescents than adults (P < 0.05, t-test).

Figure 2

Measurements of BOLD-related confounds and anatomical size of VTC and total hemispheric gray matter across age groups. (A) Motion during scan for each age group. (B) Average variance explained by the GLM model in the anatomical ROI of ventral temporal cortex (VTC) as shown in (C). The variance explained was measured for each voxel and then averaged across the ROI and across subjects. (C) Representative VTC ROI in an adolescent, OTS: occipito-temporal sulcus; CoS: collateral sulcus. (D) Average volume of the VTC in each age group. (E) Average volume of the total gray matter in each hemisphere for each age group. All bars represent the average across each age group (11 adults and 14 adolescents), error bars show standard error of the mean (SEM) for each age group. Asterisk indicates significantly higher volume in adolescents than adults (P < 0.05, t-test).

Figure 3

Face selective activations in the right fusiform gyrus for each of the 25 subjects. Face selective activations for the contrast man and boy > cars and abstract objects, P < 10⁻³, uncorrected, are projected on the inflated cortical surface of each individual from the right hemisphere for all subjects in the study. Brain images show the posterior aspect of the ventral surface of the right hemisphere as indicated by the inset in a sample brain on the right. Numbers indicate subjects’ age in years. The boundaries of the FFA are shown in black. Compass orients to anterior (A), posterior (P), right (R) or left (L). Top two rows show males’ and bottom rows show females’ brains.

Figure 4

FFA volume as a function of age and gender. (A) The volume of the FFA (man and boy > cars and abstract objects, P < 10⁻³, uncorrected) as a function of age and gender. Bars show the volume of the FFA, as defined in Figure 3, averaged across 14 adolescents (ages 12–16 years, light red) and 11 adults (18–40 years, dark red). Error bars show group SEM. Asterisks indicate significantly smaller volume than adults (P < 0.05, t-test across age groups). (B) The correlation between age and FFA volume among males and females in each hemisphere (rFFA vs. age in females: r = 0.69, P = 0.009; in males: r = 0.76, P = 0.004; lFFA vs. age in females: r = 0.48, P = 0.09; in males: r = 0.52, P = 0.08). Open triangles: males, n = 12; Filled circles: females n = 13. (C) The total volume of face selective voxels in VTC, defined as man and boy > cars and abstract objects at five different statistical thresholds (minus logarithm base 10). Volumes are measured irrespective of voxel contiguity. Light red: adolescents (ages 12–16, n = 14); dark red: adults (ages 18–40, n = 11). Error bars show group SEM (11 adults and 14 adolescents). Large asterisk indicates significantly larger volume in adults, P < 0.02, repeated measures ANOVA).

Figure 5

Average response to different stimuli and face selectivity within face selective regions of fusiform gyrus. (A) Average responses to different image categories (relative to the blank baseline) of face selective voxels during run 2. Data are averaged across 14 adolescents and 11 adults in the right hemisphere and 13 adolescents and 11 adults in the left hemisphere. Face selective voxels were independently defined using run 1 data with the contrast: man and boy > cars and abstract objects, P < 10⁻³, uncorrected. Error bars indicate SEM across subjects. Small asterisks indicate responses that are significantly less than faces (P < 0.05, t-test across subjects) and are corrected for multiple comparisons using Bonferroni correction. Large asterisk indicates significantly lower responses to faces in adolescents than adults (P < 0.05, t-test across subjects). (B) Face selectivity is plotted as a function of age. Each point represents a subject's mean t-value for the contrast faces vs. objects from run 2 data across all face selective voxels in VTC as in (A).

Figure 6

Volume of face selective activations defined using either man or boy faces. (A) Activation maps for boy selective voxels (boy faces > cars and abstract objects, P < 10⁻³), red, man selective voxels (man faces > cars and abstract objects, P < 10⁻³), green, and overlapping voxels (yellow). Data are shown for a representative adolescent brain. (B) Average volume of the cluster of voxels defined by the same contrasts as in (A). Error bars show group SEM. (C) The volume of all man selective or boy selective voxels in the VTC regardless of contiguity at five different statistical thresholds (10⁻² to 10⁻⁶, uncorrected). Light red: adolescents (ages 12–16 years, n = 14); dark red: adults (ages 18–40 years, n = 11). Error bars show group SEM. Large asterisks indicate significantly larger volume in adults vs. adolescents (P < 0.02, F-test repeated measures ANOVA).

Figure 7

Face-, object- and place selective activations in ventral cortex. (A) Face (red), object (blue) and place (green) selective activations in a representative 14-year-old subject. All activation maps are plotted at the P < 10⁻³ threshold, uncorrected. Overlapping face and object activations are shown in magenta. The spatial relation among face, object and place selective activations and also their location relative to anatomical landmarks were similar across adults and adolescents. (B) The volume of FFA, PPA and pFus/OTS averaged across 11 adults (light bars) and 14 adolescents (dark bars). Error bars indicate between subjects SEM. Asterisks indicate significantly larger volume in adults than in adolescents (P < 0.05, t-test).

Figure 8

Volume and response amplitudes of object selective activations in VTC. (A) The total volume of activated voxels for cars > scrambled, or abstract objects > scrambled at five different thresholds (10⁻² to 10⁻⁶, shown as minus logarithm base 10, uncorrected). Light red: adolescents (ages 12–16 years, n = 14); dark red: adults (ages 18–40 years, n = 11). (B) Percent signal change for object selective voxels. We defined in each subject object selective voxels in the VTC using the contrast: cars and abstract objects > scrambled, P < 10⁻³, from run 1 data. Object selective voxels were found in all subjects from run 1 data. Signal amplitudes were extracted from these voxels in run 2 data. We calculated the average response across each subject's voxels and then averaged across subjects. Error bars show group SEM (11 adults and 14 adolescents). Asterisks indicate significantly higher than scrambled (P < 0.05, t-test across subjects) and are corrected for multiple comparisons using Bonferroni correction.

Figure 9

The volume and response of place selective activations in the ventral temporal cortex. (A) The total volume of place selective activations for indoor and outdoor scenes > cars and abstract objects at five different thresholds (10⁻²–10⁻⁶, uncorrected, shown in minus log base 10 of p). Light red: adolescents (ages 12–16 years, n = 14); dark red: adults (ages 18–40 years, n = 11). (B) Response amplitudes to visual stimuli across place selective VTC voxels. Place selective voxels in the VTC were defined by the contrast scenes > objects, P < 10⁻³, in run 1. Percent signal changes were extracted from run 2 (mean and SEM). Asterisks indicate responses that significantly less than response to indoor and outdoor scenes (P < 0.05, t-test across subjects) and are corrected for multiple comparisons using Bonferroni. Error bars reflect SEM across subjects.

Figure 10

Multivoxel pattern (MVP) analysis of distributed responses to categories across the right VTC. (A) Visualization of the MVP to stimulus categories in run1 and run2 in a representative 14-year-old adolescent. (B) Group averaged Pearson correlations within and between categories from run1 versus run2. The on-diagonal components indicate the within-category reproducibility of the MVPs across runs, using different exemplars of the same stimulus category. Off-diagonal components indicate between-category correlations. (C) Summary of within-category correlations from (B). (D) Across-category correlations from (B) between faces and non-faces and between scenes and objects. Light grey: adolescents n = 11, ages 12–16 years; Dark grey: adults, n = 11, ages 18–40 years. Asterisks indicate significantly different correlations in adults vs. adolescents (P < 0.02, t-test across subjects). Error bars denote SEM across subjects.

Figure 11

Correlations between rFFA volume and recognition memory performance for faces (Red), objects (Blue) and places (Green). Diamonds: adolescents, n = 14 ages 12–16 years; Squares: adults, n = 11, ages 18–40 years.