We found evidence for prolonged development of the lPPA and rFFA, which were about three-fold larger in adults than in children ages 7–11. In children, the nascent rFFA and lPPA were associated with adult-like response amplitudes and selectivity, and were surrounded by functionally immature cortex that did not exhibit face or place selectivity. These age-related increases in rFFA and lPPA volumes were specifically associated with improvements in recognition memory for faces and places, respectively. In contrast, activation volumes for faces in the STS or objects in the LOC remained essentially constant across ages, as did recognition memory for objects. Taken together, these findings suggest that the human ventral stream undergoes a differential maturation process, whereby the LOC develops before the face- or place-selective regions of the rFFA and lPPA, which increased in size at least through age 11, in association with improved category-specific visual recognition memory.
Our controls indicated that the age-related increases in the size of the rFFA and lPPA were not due to possible confounds of developmental functional neuroimaging27,28
. First, results were not due to differences in behavioral performance during scanning. Children’s response accuracy was adult-like and their longer response times did not vary across categories during the one-back task. Second, results were not driven by potential age-dependent differences in brain size, shape or precise location of functional regions, as ROIs were defined in each subject without spatial normalization. Third, results remained similar in a subset of children and adults who were matched for several factors that could account for age-related confounds, such as subject motion, BOLD signal variability and goodness-of-fit of the GLM. Fourth, our results did not reflect age-related differences in anatomical volumes because mid-fusiform and parahippocampal volumes remained unchanged across age groups. Finally, our results were robust across a wide range of thresholds on statistical maps.
Overall, our data may explain previous failures to detect the FFA in 5–8-year-olds25
using normalized group analyses and concur with a report of smaller FFA in children (and delayed maturation relative to LOC) during viewing of movie segments of faces, places and common objects (K.S. Scherf et al
., Soc. Cog. Neurosci. Abstr. E138
2006). Developmental expansions of functional regions were correlated with developmental changes in visual recognition memory. Children performed similarly to adults in recognition-memory accuracy for objects, but showed lower accuracy for faces and places than adults. Critically, between age groups, accuracy for faces and for places correlated specifically with the volume of rFFA and lPPA, respectively. It is well established that children reach adult-like proficiency in face-recognition memory around age 16 (refs. 20,21
). Accordingly, adults outperformed adolescents, ages 12–16, in our study. However, we show here for the first time that memory for places also undergoes a prolonged development. The apparent coupling between the expansion of category-specific visual cortices and recognition-memory abilities warrants further examination for other visual and mnemonic categories29–31
and other tasks. For example, FFA responses, in particular, have been related to face detection and identification4,32
, but little is known about the development of these perceptual abilities or their relation to brain function in children.
Prolonged development of rFFA and lPPA manifested as an expansion in the spatial extent of these regions. Children’s rFFA was a third of adult size, but still evident in 85% of child subjects. Further, regardless of whether we used a clustering criterion, we found that children, compared with adults, had fewer face- and place-preferring voxels in the fusiform and PHG, respectively, rather than more spatially scattered activations for these stimuli.
In all functionally defined regions, whether smaller than or equal to adult size, children showed adult-like response magnitudes and selectivity. The smaller rFFA and lPPA in children were surrounded by cortices with adult-like responses to objects, but no selectivity for faces or places, respectively. Thus, our findings suggest that prolonged FFA and PPA development is associated with an expansion of a stimulus-selective region, by means of increased category-specific response amplitudes in an immature penumbral region.
The mechanisms underlying this expansion are unknown, but may include regional increases in the number and/or sharper tuning of face-or place-responsive neurons33
. Indeed, electrophysiological recordings in monkeys show that training to recognize novel visual stimuli increases the number of neurons responsive to the learned category in the anterior inferotemporal cortex of monkeys over periods of several months to years34
. Thus, with accumulated experience, more neurons may code for the preferred category in the penumbral regions of the rFFA and lPPA, leading to improved proficiency in face and place recognition, respectively.
Maturation of FFA and PPA regions may involve a variety of mechanisms. For example, there may be age-dependent variations in face and place viewing patterns. It has previously been found35
that atypical patterns of fixation on face parts in autism were associated with lower levels of fusiform gyrus responses to faces. There is currently no evidence indicative of differences between children and adults in patterns of fixation36
or face or place viewing. However, our findings suggest the usefulness of future developmental studies of face and place viewing patterns and their relationship to FFA and PPA responses. Additional factors that may modulate FFA responses include the level of expertise with stimuli18,19
, stimulus similarity37
and age-of-the-face stimuli (as there is evidence for a small but observable bias for better recognition of own-age faces, especially among adults38
). Future studies will be instrumental in examining the role of these factors in explaining the development of FFA responses.
The differential time course of development across high-level visual cortex varied across regions, not just perceptual categories. In children, there was a dissociation between the smaller volume of rFFA and the adult-like volumes of face-selective regions in lFFA and bilateral STS. Similarly, we found a dissociation between the smaller volume of lPPA in children and their adult-like volume of rPPA. The slower growth of the rFFA is noteworthy, as there is evidence suggesting that face processing is right-hemisphere dominant39–41
. Consistent with previous fMRI studies, the rFFA in adults was more reliably found and two-fold larger than the lFFA. Thus, the slower development of rFFA may be a limiting factor in the maturation of face perception and memory. In contrast, the more rapid maturation of STS relative to rFFA suggests that functions associated with the STS (such as processing of gaze direction and other socially communicative cues42
) may develop more rapidly than functions associated with the FFA (such as face recognition).
The PPA’s unexpected asymmetry of development is more difficult to interpret, as currently there is no evidence for hemispheric specialization for place perception. Thus, this finding awaits, and may eventually contribute to, a better understanding of PPA’s functional asymmetry.
The reasons for different rates of development in high-level visual cortex are unknown. One possibility is that the types of representations supported by rFFA and lPPA take longer to mature than those supported by LOC or STS. FFA and PPA have been implicated in holistic processing13,19,43
, which is disrupted by inversion of faces44
. Acquiring the capacity for holistic representation of a category may take longer than for feature-based representations that may occur in LOC45,46
. Second, rFFA and lPPA may retain more plasticity (even in adulthood) than LOC and STS, as at least FFA responses are modulated in adults by their level of expertise18,19
. Third, prior experience with stimuli may affect brain regions and behavior differentially, depending on stimulus category. Although all study stimuli were novel, our subjects were likely to have had more prior experience with faces than abstract sculptures. However, prior experience had little effect on LOC responses or on recognition memory in adults, which was equal for faces and objects (but worse for places). Using stimuli that are varied systematically for similarity37
and participants’ prior experience18,19,29
may further reveal the role of experience in ventral stream activations and recognition-memory performance.
Our finding of differential development across the ventral stream speaks to developmental theories of high-level vision. First, it is evident that at least some areas have a prolonged development that is not completed in early childhood. Second, our findings indicate that the entire visual ventral stream is not maturing at the same rate. Rather, there are different temporal trajectories toward reaching adult-like volumes of fMRI activation, and these trajectories seem to relate more to brain regions rather than to stimulus categories. Another implication of our data is that experience may have a more extended role in shaping the brain organization of perception and memory for faces and places than for objects. Finally, our findings form a framework for a better understanding of the normal development of high-level visual cortex in children and the neural basis of developmental disorders of face processing.