It is not currently possible to measure the real-world thought process that a child has while observing an actual school lesson. However, if it could be done, children's neural processes would presumably be predictive of what they know. Such neural measures would shed new light on children's real-world thought. Toward that goal, this study examines neural processes that are evoked naturalistically, during educational television viewing. Children and adults all watched the same Sesame Street video during functional magnetic resonance imaging (fMRI). Whole-brain intersubject correlations between the neural timeseries from each child and a group of adults were used to derive maps of “neural maturity” for children. Neural maturity in the intraparietal sulcus (IPS), a region with a known role in basic numerical cognition, predicted children's formal mathematics abilities. In contrast, neural maturity in Broca's area correlated with children's verbal abilities, consistent with prior language research. Our data show that children's neural responses while watching complex real-world stimuli predict their cognitive abilities in a content-specific manner. This more ecologically natural paradigm, combined with the novel measure of “neural maturity,” provides a new method for studying real-world mathematics development in the brain.

In the real world, children learn new information by participating in classrooms, interacting with their family and friends, and watching educational videos. While previous neuroimaging research has typically used simple tasks and short-lasting stimuli, in this study we examined brain development using a more complex and naturalistic educational stimulus. Children and adults all watched the same Sesame Street video as we measured their neural activity using functional magnetic resonance imaging (fMRI). We examined the timecourses of neural activity over the length of the video for children and adults. We found that the degree to which children showed adult-like brain responses was correlated with their math and verbal knowledge levels. In the intraparietal sulcus, children's neural correlation with adults depended on their mathematics knowledge whereas in Broca's area, it depended on their verbal knowledge. Additional experiments showed that children's neural responses in the intraparietal sulcus are selectively driven by numerical content both when children are watching Sesame Street and when they engage in a number matching task. These convergent results highlight the broad role of the intraparietal sulcus in processing numerical information. In addition, our study validates the use of naturalistic stimuli and child-to-adult neural timecourse correlations for studying brain development. We suggest that this new approach can enrich our understanding of how children's brains process information in the real world.

Copyright: © 2013 Cantlon, Li. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

As a first step toward interpreting children's real-world neural activity, we tested the relationship between children's natural viewing neural activity and their school-based knowledge. We focused on mathematics development because substantial progress has been made in characterizing the neural profile of calculation in adults [8] , [9] , children [10] – [12] , and non-human primates [13] . The data consistently indicate that regions of intraparietal cortex are more responsive during numerical processing compared to processing of other stimulus classes such as colors [14] , shapes [15] , [16] , faces, and words [16] , [17] , as well as actions such as grasping and saccadic eye movements [17] . Moreover disruption of normal functioning in intraparietal cortex through cortical lesions [18] and genetic disorders [19] is associated with selective impairments for numerical processing. Here we ask whether children show number-specific neural responses during a typical early childhood educational experience by testing the maturity of children's neural timecourses as they view educational videos. In addition, we test for a dissociation between the neural correlates of children's school-based mathematics and verbal test scores in order to examine whether there are dissociable, content-specific patterns in children's brain activity during natural viewing. Finally, we compare the neural measure derived from natural viewing with a neural measure from a traditional fMRI task to determine the relative strengths of those measures as statistical predictors of children's math performance.

Advances in developmental functional magnetic resonance imaging (fMRI) have been rapid considering that the practice of scanning children in fMRI studies began less than 20 y ago [4] . Traditional fMRI studies of category and concept development often test neural processes under conditions of maximal stimulus control (e.g., isolated pictures, tones, words, letters, or digits) with short-duration stimuli and equally short response times (i.e., 2 s). These types of studies are critical for understanding brain development, and considerable progress has been made toward understanding all aspects of brain development using a diverse array of controlled tasks in children; see [5] – [7] for review. However, the general approach of using stripped down experimental designs could present a limitation on a broad understanding of child development, as the types of thoughts that a child has in a 2-s time window with uncomplicated tasks and stimuli may not be as diagnostic of their cognitive development as how they think over long periods of time with more complex stimulation. The more traditional neuroimaging approach of using highly controlled, simple stimuli and tasks could be complemented by an approach that tests children's neural responses under more complex real-world conditions.

Naturalistic thought is an important phenomenon to understand in children who spend most of their time absorbing new information from complex scenes such as homes, schools, computers, and televisions. There is recent interest in neural activity that occurs spontaneously when people watch a natural scene or movie [1] – [3] . Naturalistic neuroimaging studies open up opportunities to collect neural measurements of children's unconstrained thoughts during real-world stimulus viewing. In this study we ask whether children's neural activity during unconstrained natural viewing of educational videos statistically predicts their performance on mathematics and verbal tests.

Results

As described in Materials and Methods, we used an intersubject correlation method [2] to measure the similarity of children's neural responses to those of adults after both groups watched the same 20-min Sesame Street video (Figure 1A). Our version of the intersubject method correlated the whole neural timecourse at every voxel in the brain between each child and a group of adults. From this correlation we derived a measure for each child of how “adult-like” or, mature, his/her pattern of neural activation was at each voxel. These maps are designated “neural maturity” maps. We performed group statistics (Fisher-transformed one sample t-tests) over the children's “neural maturity” maps (Figure 1B). The map shows regions where the similarity in neural timecourses between the children and adults while watching the video was consistently high at the group level. Broadly speaking, the children showed group-level similarity to adults in cortical regions associated with vision (occipital cortex), auditory processing (lateral temporal cortex), language (frontal and temporal cortex), visuo-spatial processing and calculation (intraparietal cortex), and several other functions. For comparison, Figure 1B also shows the mean intersubject correlation within the group of children (middle panel) and within the group of adults (right panel). The intersubject correlations among subjects reinforce claims that there are certain universals in the way that the human brain processes information [2]. We found that the intersubject correlations of children-to-adults, which we have termed “neural maturity,” increased with age. Neural maturity increased with age across large sections of the brain including basic sensory and motor cortices as well as areas of association cortex such as the intraparietal sulcus (IPS) and Broca's area (Table 1).

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larger image TIFF original image Download: Figure 1. Example stimuli and intersubject correlations. (A) Example frames from the educational television series in the natural viewing movie paradigm. (B) The average group-level intersubject correlation in BOLD time-series during the 20-min movie (Fisher transformed one-sample t-test over individual children's mean r-maps versus the group mean correlation value; FDR-corrected, q<0.01) for children correlated with adults (left), children correlated with children (middle), and adults correlated with adults (right). (C) Whole-brain statistical comparisons over intersubject correlations for children-to-adults, adults-to-adults, and children-to-children (Fisher transformed unpaired t-tests over individual subject mean r-maps). https://doi.org/10.1371/journal.pbio.1001462.g001

A whole-brain analysis comparing the intersubject correlations of children-to-adults with adults-to-adults revealed statistically higher intersubject correlations in adults-to-adults than children-to-adults predominantly in left hemisphere cortex including the left IPS, left Broca's area and the inferior and middle frontal gyri, left superior temporal sulcus, and the left fusiform and inferior temporal gyri (Figure 1C). These results complement the age-related increases in neural maturity that we report in Table 1 and indicate that neural responses that are universal among adults are still maturing in children, particularly in the left hemisphere. Interestingly, the statistical comparison of intersubject correlations for children-to-children versus children-to-adults indicated that children exhibit statistically higher intersubject correlations with other children than with adults in superior temporal cortex, predominantly in Brodmann area 22. This is an interesting finding because it suggests that there are brain regions in which children's neural responses are still immature but the pattern of neural responses is systematic among children. We also tested a whole-brain analysis comparing children-to-children intersubject correlations with adult-to-adult intersubject correlations. Children showed significantly higher intersubject correlations than did adults in superior temporal cortex along Brodmann 22. We note that the higher intersubject correlations among children in superior temporal cortex were bilateral at a slightly lower threshold than shown in Figure 1C. The fact that children show significantly higher intersubject correlations than adults in this region indicates that it not only exhibits a higher correlation among children than between children and adults but it also exhibits less between-subject variability in neural activity in childhood than in adulthood. Maps of the statistical differences in intersubject correlations between children and adults are presented in Figure 1C.

We next explored the relation between the child-to-adult intersubject correlations, which we are calling “neural maturity,” and behavior. Children were administered the TEMA-3 and KBIT-2, standardized tests for childhood mathematics and verbal/non-verbal IQ, respectively. In a voxelwise whole brain analysis, test scores were correlated with children's neural maturity values. This analysis returned a map of correlation coefficients relating individual variability in test scores with individual variability in neural maturity for the whole brain (Figure 2). These brain-behavior correlation maps represent the correlation of one standardized test while controlling for the other standardized test score in a partial correlation.

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larger image TIFF original image Download: Figure 2. Whole-brain correlation of natural viewing neural maturity and test scores. (A) Children's intersubject correlation to adults in the IPS bilaterally predicts their performance on a mathematics IQ test (TEMA), independently of their KBIT IQ test performance (whole brain analysis, cluster corrected at p<0.05, minimum 88 voxels). The figure shows regions that emerged from the whole brain correlation (top) and the mean correlation across the left and right IPS clusters (bottom). (B) Children's neural maturity in the left inferior frontal gyrus (Broca's area) predicts their performance on the KBIT verbal IQ test after regressing out their mathematics performance (TEMA). The top panel shows the results of the whole brain analysis (whole brain analysis, cluster corrected at p<0.05, minimum 65 voxels). The bottom panel shows the mean correlation across the Broca's area cluster to illustrate individual subject data. https://doi.org/10.1371/journal.pbio.1001462.g002

Figure 2A shows the resulting maps of the whole brain analysis of children's neural maturity correlated with their performance on the TEMA-3 mathematics test (controlling for their KBIT-2 scores). The data show that in bilateral regions of the IPS, children's neural maturity predicted their performance on the standardized math test, independently of how they performed on the KBIT-2 test. That is, children who performed better specifically on the math test exhibited more similar IPS responses to adults while watching the educational videos. The bottom panel of Figure 2A illustrates the average correlation between children's neural maturity values and math test scores for the left and right IPS regions of interest (ROIs). The ROI-averaged neural maturity values were calculated by taking each subject's average timecourse for the whole ROI and correlating that timecourse with the group average timecourse from the adults. The group-level correlation between the natural viewing neural timecourses of children and adults can be seen in Figure 3, which shows the raw ROI-averaged timecourses for the left and right IPS, for each group. The timecourses show comparable patterns of peak responses for children and adults across the video series in the IPS. The residual timecourses after framewise displacement (FD) correction are shown in Figure S1 for both subject groups along with the average child-to-adult correlation for each brain region.

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larger image TIFF original image Download: Figure 3. BOLD timecourses of activation from the IPS regions from adults (blue) and children (red) from the video series. The timecourses are averaged across the IPS voxels from Figure 2A. Percent signal change is calculated relative to the mean amplitude of the timecourse (the zero ordinate represents mean amplitude). The yellow bars indicate time periods where numerical information was presented in the video and the gray bars represent non-numerical video segments. The timecourses illustrate the correlation between the neural responses of children and adults. https://doi.org/10.1371/journal.pbio.1001462.g003

We tested whether our brain-behavior correlation between math test scores and IPS neural maturity could be explained by some other variable related to the scanning session. We found that the correlation between math test scores and IPS neural maturity is not explained by general memory and attention because neural maturity in those same IPS voxels did not correlate with children's scores on a general memory test about the video (left: R = −0.07, p = 0.41; right: R = 0.32, p = 0.12). In addition, the relationship between neural maturity and math test scores was not attributable to individual differences in head motion as the correlation remained significant when motion (translation and rotation) and KBIT-2 scores were simultaneously controlled (right: R = 0.67, p<0.01; left: R = 0.76, p<0.01).

We performed a parallel analysis with the standardized verbal IQ test scores (KBIT-2 verbal) to test for a functional dissociation between the mathematics and verbal domains. Figure 2B shows regions where children's neural maturity was correlated with their performance on the KBIT-2 verbal test, controlling for TEMA-3 performance. This analysis yielded a different pattern of regions including Broca's area and ventral temporal cortex. Figure 2B (bottom panel) illustrates the relationship between neural maturity and verbal test scores in Broca's area calculated from individual subjects' ROI-averaged timecourses. The correlation between verbal test scores and neural maturity in Broca's area remained significant when math test scores and motion parameters were simultaneously controlled (R = 0.68, p<0.01). Figure 4 shows the ROI-averaged timecourses for children and adults in Broca's area across the natural viewing movie sequence. Broca's area has been previously reported to respond during picture naming and verb generation tasks, consistent with our finding that it relates to children's formal verbal abilities [20]–[23]. However, the main finding is that the relationship between natural viewing neural maturity and math test scores is dissociable from the relationship between neural maturity and verbal test scores, implicating content-specific processing during natural viewing. Table 1 reports all of the brain regions that exhibited content-specific correlations between neural maturity during natural viewing and the math and verbal test scores in the whole brain analyses.

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larger image TIFF original image Download: Figure 4. BOLD timecourses of activation from Broca's area from adults (blue) and children (red) from the video series. The timecourses are averaged across the Broca's area voxels from Figure 2B. Percent signal change is calculated relative to the mean amplitude of the timecourse (the zero ordinate represents mean amplitude). The yellow bars indicate time periods where numerical information was presented in the video and the gray bars represent non-numerical video segments. https://doi.org/10.1371/journal.pbio.1001462.g004

Figure 5 shows a summary of the mean natural viewing intersubject correlation values for children-to-adults (neural maturity) and adults-to-adults in the left and right IPS and Broca's area. Adults showed a significantly higher intersubject correlation with other adults than did children with adults in all three regions, providing further evidence that the intersubject correlation during natural viewing strengthens over development (all p-values<0.001).

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larger image TIFF original image Download: Figure 5. Average intersubject correlation for adults-to-adults and children-to-adults in each of the three ROIs from Average intersubject correlation for adults-to-adults and children-to-adults in each of the three ROIs from Figure 2 : right IPS, left IPS, and Broca's area. In the top panel, intersubject correlations were calculated between each subject and the group mean (never including a subject's own data in the group mean for adult-to-adult correlations). In the bottom panel, the chart presents the correlation values when the correlation is calculated over the group mean timecourses for each region. The correlations were calculated across the 609 timepoints shown in Figures 3 and 4. https://doi.org/10.1371/journal.pbio.1001462.g005

In order to test whether the neural responses in the IPS during the natural viewing session were driven primarily by the numerical content portions of the Sesame Street video, we analyzed changes in response amplitude over the timecourses relative to the content of the movie. As mentioned earlier, Figures 3 and 4 show changes in percent signal change over the course of the movie as well as the timing of the movie content. The baseline (the zero ordinate) in Figures 3 and 4 is the mean timecourse value. We found that the right IPS region exhibited a significantly greater response amplitude during the numerical content than the non-numerical content from the video (Figure 6; t(22) = 3.58, p<0.01). The left IPS exhibited greater responses to numerical content compared to non-numerical content, but the difference was not significant. Broca's area did not exhibit a significant difference in percent signal change between numerical and non-numerical clips. Figure 6 shows the response amplitude differences between numerical and non-numerical clips for the right IPS, left IPS, and Broca's area. Importantly, we observed that the IPS intersubject correlations were not driven exclusively by these differences in amplitude between the numerical and non-numerical content because the intersubject neural maturity correlation was significant during both the numerical content and non-numerical content in both IPS regions (Fisher transformed r versus zero; left: numerical t(22) = 3.14, p<0.005, non-numerical t(22) = 4.40, p<0.001; Right: numerical t(22) = 5.23, p<0.001, non-numerical t(22) = 4.97, p<0.001). This shows that blood oxygen level dependent (BOLD) amplitude and intersubject correlation are distinct measures of brain development because neural responses are systematic and temporally correlated between subjects even during the presentation of stimuli for which the IPS does not show a selective, high-amplitude BOLD response. The implication is that there is a systematic temporal pattern even in the low-amplitude BOLD responses.

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larger image TIFF original image Download: Figure 6. Percent signal change for the numerical content versus the non-numerical content of the natural viewing video in adults and children. Percent signal change in the right IPS is significantly higher for the numerical content than the non-numerical content. The left IPS shows a marginally non-significant trend toward higher activation during numerical content than non-numerical content. Broca's area shows no difference between the numerical and non-numerical content. https://doi.org/10.1371/journal.pbio.1001462.g006

In a second experiment, we tested the same children in a more traditional fMRI paradigm to validate our natural-viewing method. In this traditional paradigm, the children were tested on a matching task with isolated pairs of faces, numbers, words, and shapes. We tested whether the ROIs that emerged from the neural maturity correlations also elicit content-specific responses during a more controlled, traditional fMRI paradigm. Figure 7A shows the children's neural response amplitudes for each of the four stimulus classes from the traditional paradigm inside the IPS ROIs that were defined as showing a relationship between children's neural maturity and math test scores during natural viewing. The data from this more traditional fMRI paradigm indicate that the IPS responded more strongly to numerical stimuli than to the three classes of non-numerical stimuli during the traditional matching task. This result accords with our finding that the maturity of children's neural responses in the IPS during educational video viewing has a biased relation to mathematics processing and is not generically related to intelligence.

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larger image TIFF original image Download: Figure 7. Cross-comparison of natural viewing and traditional task results. (A) IPS regions that exhibited a correlation between children's natural viewing neural maturity and math IQ test score also exhibited a selective response to numerical stimuli compared to face, shape, and word stimuli in a traditional fMRI paradigm. (B) And vice versa, IPS regions that exhibited a significantly greater response to the numerical stimuli in a traditional fMRI paradigm in children (numbers > faces + words + shapes, FDR corrected, p<0.05) also exhibited a significant correlation between children's neural maturity from the natural viewing paradigm and their mathematics test scores (TEMA-3). https://doi.org/10.1371/journal.pbio.1001462.g007

As described earlier, the bias for numerical processing in the IPS has been well established by several previous traditional fMRI studies with adults as well as children [8],[10],[11],[14]; see [9],[12] for review. So far no study has demonstrated a relationship between young children's neural amplitudes during traditional fMRI tests of numerical processing and their formal school-based math test performance. We tested whether children's number-related BOLD amplitudes from the traditional paradigm would predict their math test scores. We did not find a correlation between number-related amplitudes and children's math test performance in the traditional paradigm (left IPS: R = −0.17, p = 0.53; right IPS: R = −0.29, p = 0.25). This result contrasts with our findings from the natural viewing neural measures that showed a significant correlation between children's IPS activity and math performance. One explanation of the difference in results is that the content of the math-related material in the educational video is more closely related to children's school-based math skills, which results in a better correlation between the natural viewing neural data and the math test scores. This raises the possibility that neural responses to real-world stimuli might be better predictors of full-blown math development than neural responses from a simpler traditional fMRI task.

As a cross-validation of our results, we tested whether our natural viewing intersubject correlation results are maintained when the IPS is defined by activation during the traditional numerical tests. We selected the clusters of parietal voxels that elicited a statistically greater response during the traditional number task than the face, shape, and word-matching tasks (whole-brain, random effects analysis; n = 22 children; number matching > face, word, and shape matching; false discovery rate [FDR] corrected, q<0.05). These intraparietal ROIs, now defined by activation during a traditional fMRI task, showed the same partial correlation between children's math IQ scores and their neural maturity correlations during the Sesame Street video, controlling for KBIT scores (Figure 7B). Moreover, the spatial distribution of children's neural responses to numbers from the traditional task overlapped with the brain regions that showed a correlation between children's natural viewing neural maturity measures and their formal math test scores. Figure 8 shows the spatial overlap of the natural viewing and traditional task results in the IPS (whole-brain results are plotted for both datasets in Figure 8). The IPS overlap between these two maps is impressive given that one result (natural viewing neural maturity) represents the relation between children's math test scores and their child-to-adult timecourse correlations from watching Sesame Street while the other result (traditional task) represents children's neural responses to numbers over other stimulus categories from a matching task.

Finally, we used the traditional task number-related ROIs as an independent localizer to test the relationship between math test scores and the natural viewing neural responses during the numerical versus non-numerical content of the video. We tested the correlation between children's math test scores and (1) natural viewing neural maturity for the numerical versus non-numerical video content, and (2) response amplitude for the numerical versus non-numerical video content. We controlled for KBIT-2 test scores and motion in these analyses. We found that the right IPS, defined by the traditional numerical task, showed a significant correlation between math test scores and the neural maturity natural viewing correlation only for the numerical video content (one-tailed tests; numerical: R = 0.52, p<0.05; non-numerical: R = 0.37, p = 0.11). In addition, response amplitude during only the numerical content of the video was significantly correlated with children's math test scores (R = 0.63, p<0.05). Response amplitude to the non-numerical video content was negatively correlated with math test scores because of its negative correlation with response amplitude to numerical content (R = −0.63). The left IPS showed less of a distinction between numerical and non-numerical content in the correlation with math test scores as correlations for both content types were significant or marginally significant (numerical: R = 0.39, p = 0.09; non-numerical: R = 0.55, p<0.05). Response amplitude for numerical video content was also marginally correlated with math test scores in the left IPS (R = 0.37, p = 0.10).

Reviewing the neural measures from both the natural viewing and traditional paradigm, we found that the right IPS appears to be more mature than the left IPS in children. The right IPS showed a higher neural maturity score than left IPS in regions defined both by the traditional task and the natural viewing task (Fisher transformed paired t-tests; traditional: t(22) = 2.41, p<0.05; natural: t(22) = 2.74, p<0.01). The general pattern is that the temporal response pattern in the right IPS in children shows more similarity to the adult IPS than does the left IPS. Although both regions showed strong correlations between neural maturity and mathematics performance, the right IPS correlation between neural maturity and math test scores was specific to the numerical content of the video while the left IPS response was not. Compared to the left IPS, the right IPS is considered to play a greater role in the early stages of numerical development [12]. Our natural viewing data suggest that both the left and right IPS are important for mathematics development in early childhood but that the right IPS matures faster than the left IPS and its response is more selectively modulated by numerical content in early childhood.

In summary, the results from the natural viewing paradigm demonstrate that the whole timecourse of neural activation from fMRI (not just the neural amplitude) carries important information about cognitive and brain development. The data indicate that in early childhood the IPS (particularly in the right hemisphere) responds in a content-specific manner to numerical information presented naturalistically and that both the amplitude and temporal pattern of the neural response are related to children's school-based math performance. A comparison of the natural viewing and traditional paradigms shows that number-selective responses from the two paradigms overlap in parietal cortex. Both paradigms indicate content-specificity in the IPS for numerical processing in children. Yet, only the neural measures from the natural viewing paradigm correlated with children's formal school-based math performance. This suggests that some aspect of the stimulus content or measurement from the natural viewing paradigm is better able to represent the neural basis of children's early math performance than the traditional paradigm.