پاسخهای همودینامیک از کودکان مبتلا به نقص توجه و اختلال بیش فعالی (ADHD) به حالات عاطفی صورت
|کد مقاله||سال انتشار||مقاله انگلیسی||ترجمه فارسی||تعداد کلمات|
|37803||2014||8 صفحه PDF||سفارش دهید||7203 کلمه|
Publisher : Elsevier - Science Direct (الزویر - ساینس دایرکت)
Journal : Neuropsychologia, Volume 63, October 2014, Pages 51–58
Abstract Children with attention-deficit/hyperactivity disorder (ADHD) have difficulty recognizing facial expressions. They identify angry expressions less accurately than typically developing (TD) children, yet little is known about their atypical neural basis for the recognition of facial expressions. Here, we used near-infrared spectroscopy (NIRS) to examine the distinctive cerebral hemodynamics of ADHD and TD children while they viewed happy and angry expressions. We measured the hemodynamic responses of 13 ADHD boys and 13 TD boys to happy and angry expressions at their bilateral temporal areas, which are sensitive to face processing. The ADHD children showed an increased concentration of oxy-Hb for happy faces but not for angry faces, while TD children showed increased oxy-Hb for both faces. Moreover, the individual peak latency of hemodynamic response in the right temporal area showed significantly greater variance in the ADHD group than in the TD group. Such atypical brain activity observed in ADHD boys may relate to their preserved ability to recognize a happy expression and their difficulty recognizing an angry expression. We firstly demonstrated that NIRS can be used to detect atypical hemodynamic response to facial expressions in ADHD children.
1. Introduction Social cognitive deficits have been reported in school-aged children with attention-deficit hyperactivity disorder (ADHD). ADHD is characterized by inattention, hyperactivity and impulsivity, and has recently become one of the most commonly diagnosed developmental disorders in children (American Psychiatric Association, 2000). Inattention, hyperactivity, and impulsive behavior in children with ADHD can result in social problems (for review, Nijmeijer et al., 2008 and Uekermann et al., 2010). Children with ADHD experience seriously disturbed peer relations and tend to be excluded from peer activities (Hoza et al., 2005, Landau and Moore, 1991 and Owens et al., 2009). Children with ADHD have been reported to have other social cognitive impairments besides inattention, hyperactivity and impulsivity. Although we still have limited knowledge about basic face processing in children with ADHD, Tye et al. (2013) demonstrated, as far as we know, the first study to investigate the face-inversion effect and gaze processing in children with ADHD using ERP. They found that the ADHD children showed a reduced face inversion effect on P1 latency compared to TD children. Yuill and Lyon (2007) demonstrated that children with ADHD performed as well as younger controls on a non-emotional task when examiners helped children inhibit impulsive responding. However, in the same study, children with ADHD still showed impairments in the emotion understanding task that required them to choose facial photographs corresponding to emotional descriptions. Furthermore, children with ADHD and its common comorbid disorder (oppositional defiant disorder; ODD) showed significantly lower performance on an emotional understanding task than typically developing (TD) children or children with autistic disorder (Downs & Smith, 2004). These studies indicate ADHD children׳s possible cognitive difficulty in emotion understanding. School-aged children with ADHD have been found to have impaired recognition of emotional expression (Cadesky et al., 2000, Corbett and Glidden, 2000, Pelc et al., 2006, Sinzig et al., 2008 and Williams et al., 2008). Previous studies examined the recognition accuracy of children with ADHD using facial expressions of basic emotions such as anger and happiness (Cadesky et al., 2000, Corbett and Glidden, 2000, Kats-Gold et al., 2007 and Pelc et al., 2006; for review, Dickstein & Castellanos, 2012). In these studies the ADHD children recognized angry expressions less accurately than the TD children, yet recognized happy expressions as accurately as the TD children (Kats-Gold et al., 2007, Pelc et al., 2006 and Williams et al., 2008, but see also Cadesky et al., 2000). Pelc et al. (2006) asked ADHD children and TD children to identify the emotions portrayed in facial photographs of anger, happiness, disgust and sadness. Compared with the TD children, the decoding accuracy of the ADHD children was equivalent for happiness and disgust, but significantly lower for anger and sadness. Pelc et al. attributed ADHD children׳s difficulty in recognizing angry expressions to both the complex dynamics of the self-perception of anger and to a “distorted empathy” in ADHD children. Guyer et al. (2007) supported this attribution, although they found that adolescents (who were 12-years or older) with ADHD or conduct disorder performed face-emotion labeling tasks similarly to control participants, and concluded that preadolescent ADHD children could have greater difficulty recognizing facial emotions than older ADHD children. Based on these studies and the aforementioned literature reporting that school-aged ADHD children have experienced angry expressions from their peers more often than TD children (Hoza et al., 2005 and Landau and Moore, 1991), we can suppose that their biased experience may result in them processing angry expressions and happy expressions differently. The neural basis of ADHD children׳s processing of emotional expression is also different from that of TD children. When ADHD children observed a neutral expression and rated the intensity of a fearful expression, their left amygdala hyperactivated relative to that of the TD children (Brotman et al., 2010). Marsh et al. (2008) reported that when ADHD children implicitly processed a fearful expression in the gender-judgment task, their amygdala responded to a fearful expression as strongly as those of TD children, but that their posterior cingulate cortex and middle frontal gyrus hyperactivated for an angry expression. While the amygdala is recruited for the ‘amygdala network’ that is involved in triggering emotional responses to detected social stimuli, the posterior cingulate cortex and the superior temporal sulci (STS) are involved in the ‘mentalizing network’ (Kennedy & Adolphs, 2012). The STS is well-known to play important role in processing biological motion and dynamic facial movement (Allison et al., 2000 and Pelphrey et al., 2007). Also, STS is responsible for recognizing facial expression that inherent in even static image of facial expression (Andrews and Ewbank, 2004 and Engell and Haxby, 2007; Narumoto, Okada, Sadato, Fukui, & Yonekura, 2001; Said, Moore, Engell, & Haxby, 2010). The ERP study has revealed atypical neural response in the temporal region around the STS in ADHD children to an angry expression, but typical neural response to a happy expression (Williams et al., 2008). However, the spatial location of brain activity cannot be accurately drawn with ERP. To further investigate the neural activity around the STS, we can use near-spectroscopy (NIRS), which has a much more reliable spatial resolution than ERP. In this study, we used NIRS to investigate the neural basis of school-aged ADHD children׳s processing of facial expressions. NIRS has several clear advantages for studying children with developmental disorders (Ernst et al., 2012 and Fukuda, 2009; Ichikawa et al., 2014). Compared to other neuroimaging techniques such as fMRI, NIRS is completely silent, providing a non-intrusive environment and requiring less stabilization of the body and head. NIRS has been utilized in revealing the brain activity of ADHD children for executing cognitive tasks (Ehlis et al., 2008, Monden et al., 2012 and Weber et al., 2005). These studies measured the hemodynamic response in the prefrontal area. However, as mentioned above, the most important region in processing facial expressions is the occipital temporal area, including the superior temporal sulcus (STS) (Andrews and Ewbank, 2004 and Said et al., 2010). Our group previously applied NIRS to measure the brain activity in the bilateral occipital temporal area overlying the STS of 6- to 7-month-old infants while they viewed facial expressions and found face-related cerebral hemodynamic response (Nakato, Otsuka, Kanazawa, Yamaguchi, & Kakigi, 2011). For typically developed adults, it has been reported that the processing of facial expression occurs dominantly in the right hemisphere (Etcoff, 1984, Gainotti, 2012, Nakamura et al., 1999 and Tsuchiya et al., 2008). To investigate the neural basis of ADHD children׳s recognition of facial expression, we used NIRS to measure the hemodynamic responses of ADHD children and TD children to the facial expressions of happiness and anger. This is the first attempt to reveal the hemodynamic response in the bilateral occipital temporal area of ADHD and TD children to facial expressions using NIRS.
نتیجه گیری انگلیسی
Results 3.1. Group comparison We obtained hemodynamic responses from 26 boys who looked at the stimuli for more than three trials in both the happy and angry face conditions. The mean number of trials was 4.54 (SD=1.04) for the happy face condition and 4.62 (SD=.86) for the angry face condition for the ADHD boys, and 4.15 (SD=.90) for the happy face condition and 4.00 (SD=.82) for the angry face condition for the TD boys. Finally, each subject contributed an approximately equal number of trials to the analysis (for happy condition, mean 4.26, SD .92, t(24)=1.07, p=.30, n.s.; for angry condition; mean 4.35, SD .89, t(24)=1.59, p=.13, n.s). We conducted a 2×2 ANOVA on the number of trials contributed by each subject with group (ADHD versus TD) as a between-participant factor and condition (happy face versus angry face) as a within-subject factor and found no significant main effect or interaction in the number of trials between the ADHD and TD groups. Fig. 2 shows the time course of the average change of the oxy-Hb and deoxy-Hb concentrations during the presentation of the happy and angry faces. The grand-averaged data obtained by all 13 subjects of each subject group were shown to examine the general tendency of inter-hemispheric difference. Fig. 3 shows the mean Z-score from 5 to 15 s of the trial in the left and right temporal areas. We obtained the data of oxy-Hb and deoxy-Hb and analyzed them separately. Mean Z-score of oxy-Hb (panel A) and deoxy-Hb (panel B) change from 5 to 15s of ... Fig. 3. Mean Z-score of oxy-Hb (panel A) and deoxy-Hb (panel B) change from 5 to 15 s of the trial. In each panel, the vertical lines in the graphs represent 1 SEM. In the ADHD group, ANOVA with condition (happy face versus angry face) and measurement area (right versus left) revealed a significant main effect of condition. The concentration of oxy-Hb in the right temporal area increased significantly only for happy faces (a darker bar) compared to the chance level of 0 (⁎p<.05). In the TD group, ANOVA with condition and measurement area revealed a significant main effect of measurement area. The concentration of oxy-Hb in the right temporal area increased significantly for both the happy (a darker bar) and angry faces (a pale bar) compared to the chance level of 0 (⁎p<.05). Figure options To compare the differential oxy-Hb concentration between the ADHD and TD groups, a 2×2×2 ANOVA was conducted with: (i) group (ADHD versus TD) as a between-participant factor, (ii) condition (happy face versus angry face) as a within-subject factor, and (iii) measurement area (right versus left) as a within-subject factor. This analysis revealed a significant interaction between group and condition, F(1,24)=5.152, p=.03, partial η2=.18 and a significant main effect of measurement area, F(1,24)=12.01, p=.002, partial η2=.33. The other main effect and the other interactions were not significant, p>.10. For deoxy-Hb concentrations, the ANOVA revealed a significant main effect of measurement area, F(1,24)=4.58, p =.04, partial η2=.16. The other main effect and the other interactions were not significant, p>.10. As a follow-up test, we tested the effect of condition by independent two-sample t-tests on oxy-Hb concentration of ADHD and that of TD. We found that ADHD children showed increased oxy-Hb concentration for happy faces similarly as TD children did, t(24)=.20, p=.84, r=.04, while for angry faces they showed less oxy-Hb concentration than TD children did, t(24)=3.97, p=.001, r=.63. For deoxy-Hb concentrations, the ANOVAs did not reveal any significant effect or interaction, p>.10. Furthermore, as we originally aimed to illustrate the differential hemodynamic lateralization between the groups, we conducted 2×2 ANOVAs respectively with: (i) condition (happy face versus angry faces) and (ii) measurement area (right versus left) as within-subject factors. For the oxy-Hb concentrations of the ADHD boys, this analysis revealed only a significant main effect of condition, F(1,12)=6.53, p=.03, partial η2=.35; no other main effects or interactions were significant 2. On the other hand, for the oxy-Hb concentrations of the TD boys, only a main effect of measurement area was significant, F(1,12)=11.74, p=.01, partial η2=.49; no other main effects or interactions were significant. For deoxy-Hb concentrations, the ANOVAs did not reveal any significant effect or interaction, p>.10. To examine the possibility that there was differential activity for the presentation of faces compared with the baseline, we conducted a two-tailed one-sample t-test on the Z-scores against a chance level of 0 (baseline) for each condition and measurement area (happy-right, happy-left, angry-right, and angry-left). Multiple comparisons were corrected using a false discovery rate (FDR), q=.05. The analysis revealed that the ADHD boys showed significant hemodynamic response only to the happy face condition. Their increase of oxy-Hb and decrease of deoxy-Hb in the right hemisphere were significant, oxy-Hb; t(12)=3.25, p=.01, deoxy-Hb; t(12)=−5.32, p =.00, but not in the left hemisphere, oxy-Hb; t(12)=1.76, p=.10, deoxy-Hb; t(12)=−1.98, p =.07. On the other hand, the TD boys showed significant hemodynamic response to both the happy face and angry face conditions only in the right hemisphere. The oxy-Hb of the TD boys was significantly increased in the right hemisphere for the happy face condition, t(12)=2.846, p=.02, and for the angry face condition, t(12)=4.506, p=.00. In addition, deoxy-Hb decreased significantly in the right hemisphere for both the happy face condition, t(12)= −2.84, p=.02, and the angry face condition, t(12)=−3.36, p=.01, and in the left hemisphere for the happy face condition, t(12)=−2.41, p=.03. 3.2. Individual differences in peak latency To further investigate group differences between the ADHD and TD groups, we compared the mean and variance of the individual differences in peak latency of the hemodynamic responses. Fig. 4 shows the individual data for the oxy-Hb time course averaged across the trials. First, we conducted two-tailed two-sample t-tests on the peak latencies for each condition and hemisphere; however, we did not find any significant differences. Next, we conducted Levene׳s tests for equality of variances and found that the peak latency had a significantly broader deviation for the ADHD group than for the TD group in the right temporal area under both the happy face condition, F=8.14, p=.01, and the angry face condition, F=6.87, p=.02. The individual difference in the latency of peak hemodynamic response deviated with broader temporal range in the ADHD group, while that of the TD group gathered at 14–17 s after stimuli onset. Because we did not find any difference in the number of trials and channels contributed by participants from each group, we could conclude that the variance of peak latency was not caused by a difference in the amount of data acquired from the ADHD and TD groups. The time course of oxy-Hb change in individual subjects. In each graph, line ... Fig. 4. The time course of oxy-Hb change in individual subjects. In each graph, line plots indicate the Z-score of individual data averaged across trials. Markers (of diamonds for the ADHD group and circles for the TD group) on each line indicate the peak of the concentration of oxy-Hb. The box plot displays the distribution of individual peak latency.