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. 2007 Apr;10(4):512-22.
doi: 10.1038/nn1865. Epub 2007 Mar 11.

Differential development of high-level visual cortex correlates with category-specific recognition memory

Golijeh Golarai  1 , Dara G Ghahremani, S Whitfield-Gabrieli, Allan Reiss, Jennifer L Eberhardt, John D E Gabrieli, Kalanit Grill-Spector
Affiliations

Differential development of high-level visual cortex correlates with category-specific recognition memory

Golijeh Golarai et al. Nat Neurosci. 2007 Apr.

Abstract

High-level visual cortex in humans includes functionally defined regions that preferentially respond to objects, faces and places. It is unknown how these regions develop and whether their development relates to recognition memory. We used functional magnetic resonance imaging to examine the development of several functionally defined regions including object (lateral occipital complex, LOC)-, face ('fusiform face area', FFA; superior temporal sulcus, STS)- and place ('parahippocampal place area', PPA)-selective cortices in children (ages 7-11), adolescents (12-16) and adults. Right FFA and left PPA volumes were substantially larger in adults than in children. This development occurred by expansion of FFA and PPA into surrounding cortex and was correlated with improved recognition memory for faces and places, respectively. In contrast, LOC and STS volumes and object-recognition memory remained constant across ages. Thus, the ventral stream undergoes a prolonged maturation that varies temporally across functional regions, is determined by brain region rather than stimulus category, and is correlated with the development of category-specific recognition memory.

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Conflict of interest statement

COMPETING INTERESTS STATEMENT

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1
Behavioral data during scan. Accuracy (a) and response times (b) in a one-back task during the scan, for faces, abstract sculptures, scenes and textures (scrambled objects). Light gray, children ages 7–11; dark gray, children ages 12–16; black, adults. Error bars show s.e.m. for each age group.
Figure 2
Figure 2
Face-selective activations in the fusiform gyrus as a function of age. (a) The FFA was defined as faces > objects (P < 10−3, uncorrected). Blue lines point to the rFFA in coronal, sagittal and horizontal views from a representative adult subject. (b) Same as a, but data are from a representative 8.8-year-old child. (c) Left, lFFA volume; right, rFFA volume. Bars show the volume of the FFA, as defined in (a,b), averaged across 20 children aged 7–11 (light gray), 10 adolescents aged 12–16 (dark gray) and 15 adults (black). Error bars show group s.e.m. Red bars show data from groups that were matched for BOLD-related confounds (Supplementary Note 1), and include 10 children, 9 adolescents and 13 adults. * Children < adults; P < 0.02. (d) The volume of anatomically defined mFG. Bars represent data as in c. (e) The total number of face-selective voxels (faces > objects) within the anatomically defined left or right mFG (anatomical ROIs in d), regardless of contiguity, were plotted against the minus logarithm (base 10) of six statistical thresholds (10−1 to 10−6, uncorrected) for a subset of subjects, who were matched for BOLD-related confounds in mFG in each age group. Circles, children (ages 7–11, n = 10); squares, adolescents (ages 12–16, n = 9); triangles, adults (n = 13). Error bars show s.e.m for each age group.
Figure 3
Figure 3
BOLD response amplitudes in the FFA and face selectivity. (a,b) Percent BOLD signals relative to fixation background for each image category and age-group in the left (a) and right (b) hemisphere. Bars represent data as in Figures 1 and 2. (c,d) Average face selectivity (face − object)/(face + object), is plotted for age groups matched for BOLD-related confounds (Supplementary Note 1) in the left (c) and right hemisphere (d). Positive values along the y-axis indicate preference for faces, negative values preference for objects. Circles, children (ages 7–11); squares, adolescents (ages 12–16); triangles, adults. Error bars show group s.e.m. (c) Average face selectivity in a series of concentric ROIs (constant-sized across subjects) in the left hemisphere: P, voxel with the highest t-value for faces > objects in mFG (lFFA peak); 3P, similarly, three contiguous voxels with the highest t-values. Three spherical ROIs were centered at the lFFA peak in each subject, and sized to match the group average lFFA size in children (Child), adults (Adult) and 150% of the average lFFA size in adults (150%). (d) Average face selectivity in a series of concentric spherical ROIs (P, 3P, Child, Adult and 150%) were defined as in (c), but centered on the rFFA peak. Three additional concentric shell ROIs were created as the region in Child excluding 3P (ROI 3), Adult excluding Child (ROI 5) and 150% excluding Adult (ROI 7). Yellow arrow: face selectivity was significantly lower among children (n = 10) than among adults (n = 13), in the shell representing the penumbral region of the rFFA in children (ROI 5, P < 0.05). (e) Percent BOLD amplitude for faces and objects versus fixation baseline in the penumbral region of rFFA in children (ROI 5, * children < adults, P < 0.05). Data are presented as in (a). Error bars show group s.e.m.
Figure 4
Figure 4
Face-selective activations in the STS as a function of age. (a) The STS was defined in the posterior aspect of the superior temporal sulcus, as a cluster of contiguously activated voxels that responded more strongly to faces than to objects (P < 10−3, uncorrected). Blue lines point to the rSTS in activation maps from the same representative adult subject as in Figure 2a. (b) Analogous to a, but data are from the same 8.8-year-old child as in Figure 2b. (c) Average volume of the functionally defined STS (as in a and b) across children (n = 20), adolescents (n = 10) and adults (n = 15). (d) Average BOLD response amplitudes in STS across stimuli and age groups. Bar graphs represent age groups as in Figure 1. Error bars show group s.e.m.
Figure 5
Figure 5
Object-selective activations in the LOC as a function of age. (a) The LOC was defined in each lateral occipital cortex, as a cluster of contiguously activated voxels that responded more to objects than textures (P < 10−5, uncorrected). Blue lines point to the rLOC from the same representative adult subject as in Figure 2a. (b) Analogous to a, but data are from the same 8.8-year-old child as in Figure 2b. (c) Average volume of the functionally defined LOC (as in a and b) across age groups. (d) Average BOLD response amplitudes in the LOC for each age group and category. Bar graphs represent age groups as in Figure 1. Error bars show group s.e.m.
Figure 6
Figure 6
Place-selective activations in the PHG as a function of age. (a) The PPA was defined as places > objects (P < 10−4 uncorrected). Blue lines point to the lPPA in activation maps from the same representative adult subject as in Figure 2a. (b) Analogous to (a), but data are from the same 8.8-year-old child as in Figure 2b. (c–e) Gray scale bars represent age groups as in Figure 2. Red bars represent data from groups that were matched for BOLD-related confounds in PHG (Supplementary Note 1; right, 10 children, 9 adolescents and 11 adults; left, 10 children, 9 adolescents and 12 adults). Error bars show group s.e.m. (c) Left, lPPA volume (* children < adults; P < 0.05); right, rPPA volume. (d) The volume of anatomically defined PHG in each hemisphere. (e) The total number of place-selective voxels (places > objects) within the anatomically defined left and right PHG (anatomical ROIs in d), regardless of contiguity, were plotted against the minus logarithm (base 10) of six statistical thresholds (10−1 to 10−6, uncorrected) for the subset of subjects who were matched for BOLD-related confounds in the PHG in each age group. Circles, children (ages 7–11, n = 10); squares, adolescents (ages 12–16, n = 9); triangles, adults (n = 13). Error bars show group s.e.m.
Figure 7
Figure 7
BOLD response amplitudes in the PPA and place selectivity. (a,b) Percent BOLD signals relative to fixation background for each image category and age-group in the left (a) and right (b) hemisphere. (c,d) Average place selectivity, (place − object)/(place + object), in concentric ROIs (constant-sized across subjects) is plotted for age groups matched for BOLD-related confounds in the PHG (Supplementary Note 1) in the left (c) and right hemisphere (d). (c)Average place selectivity in a series of concentric ROIs (constant-sized across subjects, ROI 1 to 8) centered at the lPPA peak in each subject. Spherical ROIs were sized to match the group averaged lPPA size in children (Child) and in adults (Adult) and 150% of the average lPPA size in adults (150%). Shell ROIs were defined as the region in Child excluding 3P (ROI 3), Adult excluding Child (ROI 5) and 150% excluding Adult (ROI 7 ). Yellow arrow: place selectivity was significantly lower among children (n = 10) than among adults (n = 12), in the shell representing the penumbral region of the lPPA in children (ROI 5, P < 0.01). (d) Average place selectivity in a series of concentric ROIs (ROI 1 to 5) as in (c), but centered at the peak of the rPPA in individual subjects and relative to the average size of the rPPA in children and adults. Place selectivity was not statistically different among the age groups, for any of these ROIs in rPPA. (e) Average BOLD response amplitudes to places and objects within the ROI representing the penumbral region of the lPPA in children (ROI 5, children < adults, *P < 0.05). Error bars show group s.e.m.
Figure 8
Figure 8
Performance of different age groups on an independent recognition-memory test for faces, abstract sculptures and places. (a) Recognition accuracy (percent accuracy = (hit − false alarm)/total) for faces, places and objects. Face-recognition-memory performance in adults was higher than children’s (*P < 0.0001) or adolescents’ (**P < 0.03). Adolescents’ face-recognition-memory performance was higher than children’s (**P < 0.03). Place-recognition-memory performance in adults was higher than children’s (†P < 0.0001). Adolescents’ memory for places was higher than children’s (‡P < 0.01). Error bars show group s.e.m. (b) Correlations for face-recognition memory and rFFA size are shown for each age group. (c) Correlations for place-recognition memory and lPPA size are shown for each age group. (d,e) Correlations for object-recognition memory and right or left LOC size are shown for each age group.
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