School-age children with attention deficit hyperactivity disorder (ADHD) have difficulties in interpersonal relationships, in addition to impaired facial expression perception and recognition. For successful social interactions, the ability to discriminate between familiar and unfamiliar faces is critical. However, there are no published reports on the recognition of familiar and unfamiliar faces by children with ADHD.
We evaluated the neural correlates of familiar and unfamiliar facial recognition in children with ADHD compared to typically developing (TD) children. We used functional near-infrared spectroscopy (fNIRS) to measure hemodynamic responses on the bilateral temporal regions while participants looked at photographs of familiar and unfamiliar faces. Nine boys with ADHD and 14 age-matched TD boys participated in the study. fNIRS data were Z-scored prior to analysis.
During familiar face processing, TD children only showed significant activity in the late phase, while ADHD children showed significant activity in both the early and late phases. Additionally, the boys with ADHD did not show right hemispheric lateralization to familiar faces.
The early development of facial processing has been considered fundamental to the development of social abilities and theory of mind [5]. Several abilities compose social cognition, including the ability to perceive the emotions of another person from affective prosody, faces, and body posture [4]. It has been shown repeatedly that children with ADHD, particularly those that are school-age, have impaired facial expression perception and recognition [4, 6, 7].
However, there is limited knowledge regarding basic facial processing in ADHD. Tye et al. (2013) were the first to explore the face inversion effects and gaze processing in children with ADHD using event related potentials (ERPs) [8]. They found that children with ADHD displayed a reduced face inversion effect on P1 latency compared with TD children. Sinzig et al. (2008) reported that the ability of facial affect recognition is reduced in children suffering from ADHD symptoms, both in autistic and ADHD children [9]. Several lines of evidence have suggested differential processing between familiar and unfamiliar faces with behavioral as well as neural findings in typical adult studies [10, 11]. Therefore, we hypothesized that ADHD children, who present with social cognitive impairments, may have different familiar and unfamiliar facial recognition compared with TD children.
resolution, and provides a non-intrusive environment requiring less restriction of the body and head [7, 20]. fNIRS has been adopted in studies examining the brain activity of children with ADHD while they perform cognitive tasks [16,17,18,19, 21]. These studies measured the hemodynamic response in the prefrontal areas, which play an important role in processing executive cognitive functions. With regard to facial recognition, fNIRS also has been utilized to measure neural activities in the temporal area, including the superior temporal sulci (STS), which is known to play an important role in processing faces [22]; this is consistent with other hemodynamic evidence of facial processing in the temporal cortex of the brain [7, 20, 23,24,25,26,27].
To our knowledge, there are no published reports on the recognition of familiar and unfamiliar faces in children with ADHD. Thus, the purpose of this study is to compare the neural correlates involved in familiar (mother) and unfamiliar facial recognition in children with and without ADHD using a fNIRS system, which was placed over the bilateral temporal regions.
Data from the 23 boys who looked at faces over more than three trials in both the familiar face and unfamiliar face conditions were obtained. Available trials were averaged across trials for each condition (familiar face, mean 5.06, SD 0.89; unfamiliar face, mean 4.97, SD 0.95). The mean number of removed trials for the familiar face condition was 0.33 (SD 0.74) while that for the unfamiliar face condition was 0.30 (SD 0.64). There was no significant difference between the numbers of available trials under each condition.
The current study compared the neural correlates of viewing familiar and unfamiliar facial images in ADHD and TD boys using fNIRS. To measure the neural activities of facial recognition, the fNIRS probes were set on the bilateral temporal regions, including on the STS, which plays an essential role in processing faces. These measuring procedures were the same as in previous studies [7, 20, 23,24,25,26,27]. We calculated the Z-scores for the 12 channels within the temporal area from the raw data in the familiar and unfamiliar face conditions.
fNIRS monitors blood volume and oxygenation in the brain. In this study, the hemodynamic response, as indicated by oxy-Hb, increased gradually during the test period in both groups and was found to occur predominantly in the right hemisphere in TD boys. Neuroimaging studies have reported that the major aspects of facial processing arise predominantly in the right hemisphere [30, 31]. Therefore, these findings suggest that the hemodynamic response in this study indicates facial recognition in ADHD and TD boys. In the familiar face condition, Z-scores of oxy-Hb concentrations were significantly increased in the early and in the late phase for ADHD boys. In contrast, for TD boys, significant changes were only found in the late phase. In the unfamiliar face condition, we found no significant changes in either group of boys. This indicates that the hemodynamic response in ADHD boys to familiar faces may be earlier than TD boys. However, this research finding may not be related to the major ADHD symptoms of hyperactivity, impulsivity, and inattention. Gobbini et al. documented that familiar faces are recognized by processes that operate outside the focus of attention and without visual awareness [32]. In addition, numerous studies have reported slower reaction time variability among individuals with ADHD compare to TD individuals [33, 34]. Another possibility is that the ADHD boys did not show adaptation for familiar faces. Generally, repeated facial presentation induces neural adaptation [35].
Hemodynamic responses to familiar faces were found to occur predominantly in the right temporal area in TD boys. In contrast, ADHD boys showed significantly increased concentration of oxy-Hb to familiar faces in both the right and left temporal areas compared with the baseline. The TD boys showed right hemispheric dominance in processing faces, which is consistent with many other neuroimaging studies [30, 31]. Whereas the right hemispheric dominance in TD boys was indicated and successfully monitored by fNIRS, ADHD boys did not show right hemispheric lateralization to familiar faces. This finding is consistent with previous studies [6, 7]. Ichikawa et al. showed that the brain activity stimulated by seeing a happy face is significantly increased in both the right and left temporal areas compared with the baseline in ADHD boys.
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Participants felt discomfort toward all three types of faces with dots, that is, faces with black dots, gray dots, and both. However, interestingly, participants felt less discomfort when both black and gray dots were presented on the face than when only black dots were presented. The participants perceived depth between the black dots and the face in 85% of the trials with black dots and shadow-like gray dots, and there was a significant correlation between discomfort and frequency of depth perception. However, in the trials with black dots only and gray dots only, they perceived depth in only 18% and 27% of the trials, respectively, and the correlations between the frequencies of depth perception and discomfort were not significant.
The spatial relationship between the dots and the background face also plays a role in the generation of discomfort. Viewers felt more discomfort toward dots on upright faces than on inverted faces [6]. However, it was still not clear how the perceived spatial relationship between the dots and the background face plays a role in the generation of discomfort. In previous studies, the dots were placed directly on background faces or objects, making them physically and perceptually attached to the background faces or objects. To separate the perceived spatial relationship from the physical relationship in the present study, we inserted shadow-like gray dots between the foreground black dots and the background face (see Fig. 1). Since the time of Leonardo da Vinci, it has been widely understood that cast shadows evoke a sense of depth [15,16,17]. If trypophobic discomfort simply depends on the number of dots, viewers would feel more discomfort toward a face that has both black dots and gray dots than they do toward a face with only black or gray dots. However, if the discomfort also depends on the perceived spatial relationship between the dots and face, we hypothesized that viewers would feel less discomfort toward the face with black dots and gray dots, as the presence of the gray dots allows the black dots to be perceived as separate from the face. We tested these hypotheses through a subjective discomfort rating experiment.
The results also suggest that the physical stimulus characteristics such as contrast energies in the lower medium spatial frequency ranges, and local luminance between the dots and the background faces might explain the discomfort to some extent. However, spatial frequency could not fully explain the results because there were some inconsistencies between the contrast energies and discomfort evaluation. Local contrast between the dots and the background faces could not explain the results fully either, because the black and gray dots stimulus had contrasts for both black and gray dots but the discomfort rating was not the strongest.
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