Neither Enhanced Nor Lost: The Unique Role of Attention in Children's Neural Representations

Abstract

A defining feature of children's cognition is the especially slow development of their attention. Despite a rich behavioral literature characterizing the development of attention, little is known about how developing attentional abilities modulate neural representations in children. This information is critical to understanding how attentional development shapes the way children process information. One possibility is that attention might be less likely to shape neural representations in children as compared with adults. In particular, representations of attended items may be less likely to be enhanced relative to unattended items. To investigate this possibility, we measured brain activity using fMRI while children (seven to nine years; male and female) and adults (21-31 years; male and female) performed a one-back task in which they were directed to attend to either motion direction or an object in a display where both were present. We used multivoxel pattern analysis to compare decoding accuracy of attended and unattended information. Consistent with attentional enhancement, we found higher decoding accuracy for task-relevant information (i.e., objects in the object-attended condition) than for task-irrelevant information (i.e., motion in the object-attended condition) in adults' visual cortices. However, in children's visual cortices, both task-relevant and task-irrelevant information were decoded equally well. What is more, whole-brain analysis showed that the children represented task-irrelevant information more than adults in multiple regions across the brain, including the prefrontal cortex. These findings show that (1) attention does not modulate neural representations in the child visual cortex, and (2) developing brains can, and do, represent more information than mature brains.SIGNIFICANCE STATEMENT Children have been shown to struggle with maintaining their attention to specific information, and at the same time, can show better learning of "distractors." While these are critical properties of childhood, their underlying neural mechanisms are unknown. To fill in this critical knowledge gap, we explored how attention shapes what is represented in children's and adults' brains using fMRI while both were asked to focus on just one of two things (objects and motion). We found that unlike adults, who prioritize the information they were asked to focus on, children represent both what they were asked to prioritize and what they were asked to ignore. This shows that attention has a fundamentally different impact on children's neural representations.

Keywords: attention; cognitive neuroscience; development; fMRI.

Figure 1.

Stimuli and procedure of the experiment and behavioral performance. A, Object and motion stimuli. As shown in B, each 2-s trial consisted of one object with superimposed dots moving in one motion direction; for the object task condition (first row), participants were instructed to detect objects that repeated from the previous trial and ignore any possible repeats in motion; for the motion task (second row), participants were asked to detect repeating motion directions from the previous trial and ignore any possible object repeats. In each subsequent graph (C–F), adults' (in blue) and children's (in green) task performance, averaged across the task conditions, is plotted on the left, and their performance in each task condition is plotted on the right. Each colored dot indicates the mean of each group and the line indicates the estimated confidence interval (95%). Individual data are plotted in small colored dots. C, Sensitivity to target (repeats in the attended domain; d prime) for adults (in blue) and for children (in green) in object and motion task conditions, z(hit rate) – z(false alarm to all nontarget trials). D, Reaction time in object and motion task conditions for adults (in blue) and children (in green). E, False alarms to repeats in the unattended domain (e.g., responding to repeats in motion in object task). F, Sensitivity to repeats in the attended domain, based on hit rate and false alarms to repeats in the unattended item (E), z(hit rate) – z(false alarm to unattended domain), ***p < 0.001, *p < 0.05, n.s. p > 0.05.

Figure 2.

A subset of adults (n = 13; plotted in light blue) whose FA values are matched to those in children (plotted on the right; children's data are plotted in green) showed similar patterns of decoding as the full adult sample (plotted in darker blue). n.s. p > 0.05.

Figure 3.

Univariate analyses showing the contrast between the object task (e.g., attending to the objects) and the baseline task (left), and the contrast between the motion task (e.g., attending to motion) and the baseline task (right), in adults (upper panel), and in children (lower panel). Adult show greater activation when attending to either object or motion in fronto-parietal regions, including the middle frontal gyrus (MFG), the frontal eye field (FEF), and the superior parietal lobule, and also in visual cortex. In children, the MFG shows greater activation in the object task. The MFG, the FEF, and the visual cortex show greater activation when attending to motion.

Figure 4.

Decoding of object and motion in regions of interest. A, The lateral occipital cortex (LOC) is visualized, and all data plotted in this top panel (B, C) are from this region of interest. In B and C, decoding accuracy is plotted for objects (B) and motion directions (C), separately for adults and children (x-axes) when each stimulus class (objects in B, motion in C) is attended (red) or unattended (blue). Since the LOC is selective for object information, the object data are highlighted by the inclusion of a pink box around graph B. Decoding accuracy that is significantly greater than chance level is marked at the bottom of the plot (***p < 0.001, **p < 0.01, *p < 0.05), and significant comparisons between adults and children as well as their interactions with task condition are noted at the top of each plot (*p < 0.05). Individual data are plotted as small opaque dots, and error bar indicates SEM. For object decoding, greater decoding of attended information observed only for adults but not in children in LOC (C), and this interaction between group and attention condition is not observed for motion (C). D, The middle temporal area (MT) is visualized, and all data plotted in the bottom panel (E, F) are from this region of interest. In E and F, decoding accuracy is plotted for the four objects (E) and the four motion directions (F), separately for adults and children (x-axes) when each stimulus class was attended (red) or unattended (blue). In the MT, we observe successful decoding of motion directions only when motion was task-relevant in adults. However, children's MT represent motion both when motion was task-relevant or irrelevant.

Figure 5.

Comparison of searchlight maps between adults and children. Blue clusters indicate better decoding in adults than children, and green clusters indicate better decoding in children than adults. A, Contrast between adults and children for attentional modulation (attended–unattended; both for object and motion). B, C, Contrast between adults and children for attended (B) and unattended (C) searchlight maps (both for object and motion). Both maps are thresholded at p < 0.05 and cluster-wise correction was conducted for multiple comparisons (minimum cluster size, 226 voxels).