Typical and Atypical Development of Functional Connectivity in the Face Network

Abstract

Extensive studies have demonstrated that face recognition performance does not reach adult levels until adolescence. However, there is no consensus on whether such prolonged improvement stems from development of general cognitive factors or face-specific mechanisms. Here, we used behavioral experiments and functional magnetic resonance imaging (fMRI) to evaluate these two hypotheses. With a large cohort of children (n = 379), we found that the ability of face-specific recognition in humans increased with age throughout childhood and into late adolescence in both face memory and face perception. Neurally, to circumvent the potential problem of age differences in task performance, attention, or cognitive strategies in task-state fMRI studies, we measured the resting-state functional connectivity (RSFC) between the occipital face area (OFA) and fusiform face area (FFA) in human brain and found that the OFA-FFA RSFC increased until 11-13 years of age. Moreover, the OFA-FFA RSFC was selectively impaired in adults with developmental prosopagnosia (DP). In contrast, no age-related changes or differences between DP and normal adults were observed for RSFCs in the object system. Finally, the OFA-FFA RSFC matured earlier than face selectivity in either the OFA or FFA. These results suggest the critical role of the OFA-FFA RSFC in the development of face recognition. Together, our findings support the hypothesis that prolonged development of face recognition is face specific, not domain general.

Keywords: development; developmental prosopagnosia; face recognition; fusiform face area; occipital face area; resting-state functional connectivity.

Figure 1.

Behavioral development of face-specific recognition ability. A, Example stimuli and trial types in the old/new recognition task. In the study segment, participants studied a series of images of either faces or flowers. In the test segment, the studied images were shown with new images from the same category intermixed. Participants were asked to indicate which of the images had been shown in the study segment. B, Scatter plot showing correlation between age and face memory and a histogram showing the number of participants at each age. C, Scatter plot showing correlation between age and object memory. D, Scatter plot showing correlation between age and face-specific memory (regressing out the variance of flower memory from that of face memory). E, Example stimuli and trial types in the discrimination task. In each trial, a frontal-view image and a three-quarter-view image of either a face or a 3D asymmetrical assemblage of cubes were presented successively. Participants were asked to indicate whether the second image was of the same face/cubes as the first. F–H, Scatter plots showing the correlation between age and face discrimination (F), object discrimination (G), and face-specific discrimination (regressing out the variance of object discrimination from that of face discrimination) (H).

Figure 2.

Development of RSFC in the ventral visual pathway. A, Face- and object-selective regions centered at averaged Talairach coordinates across child participants. The face-selective regions OFA and FFA (p < 10⁻⁴, uncorrected, red) and the object-selective regions LO and pFs (p < 10⁻⁴, uncorrected, green) are shown on an inflated right hemisphere of MNI standard template. Sulci are shown in dark gray and gyri in light gray. B, Scatter plots of the correlation between OFA-FFA RSFC and age. C, Scatter plots of the correlation between LO-pFs RSFC and age. D, Magnitude of Pearson's correlation coefficients between RSFCs in the ventral pathway and age.

Figure 3.

Deficits in behavioral performance and disruption of RSFC in DP. A, Top, Example stimuli and trial types in the identification task on faces and objects. Participants reported the prespecified targets at the subordinate level: Chiu-Wai Leung (a famous Chinese movie star), chrysanthemum, pigeon, and jeep. Bottom, Accuracies of normal adults and DP subjects in the face- and object-identification tasks. B, Top, Example stimuli and trial types in the whole-part task. Participants identified a face part of one individual (nose, mouth, or eyes) presented either in the context of the whole face or in isolation (part). Bottom, Accuracies of normal adults and DP subjects in the whole-part task. C, Magnitude of OFA-FFA RSFC and LO-pFs RSFC in normal adults and DP subjects. D, Magnitude of OFA-FFA RSFC in the DP subjects, children 7–10 years of age, children 11–13 years of age, and normal adults. Error bars indicate SEM. *p < 0.05; **p < 0.001.

Figure 4.

Different developmental trajectories of functional connectivity and face selectivity in the face system. A, Face selectivity in the OFA and FFA in children 7–10 years of age, children 11–13 years of age, normal adults, and DP subjects. B, Magnitude of face selectivity and object selectivity in children and normal adults. The OFA and FFA were averaged for face selectivity and the LO and pFs were averaged for object selectivity. C, Schematic summary showed that the development the OFA-FFA RSFC preceded the development of face selectivity. For children 7–10 years of age, both the RSFC and face selectivity were developing. For children 11–13 years of age, the RSFC was comparable to adult levels, whereas face selectivity was still developing. D, Magnitude of face selectivity and object selectivity in the DP subjects and normal adults. Error bars indicate SEM. *p < 0.05.