خلفی P1 و فرونتال منفی بازتاب دهنده تغییرات رشدی در حواس پرتی توجه در دوران بلوغ

Abstract Previous studies in adults have revealed that attentional distraction modulates the late positive potential (LPP) during emotion regulation. To determine whether early visual components reflect developmental changes in attentional distraction during adolescence, we collected event-related potentials from 20 young adolescents, 18 older adolescents, and 18 young adults as they performed a distraction task (counting) while viewing affective images. Consistent with previous findings obtained in distraction studies, the distraction task (counting) reduced emotional modulation of the LPP. At an early stage of processing, counting reduced emotional modulation of P1 and increased the negativity bias of early frontal negativity (eFN) for negatively valenced pictures compared to simple viewing with no distraction. sLORETA analyses further revealed eFN indexing of rostral prefrontal cortical activation, a cortical area that has been shown in recent fMRI studies to be activated by distraction. Moreover, P1 amplitudes in young and older adolescents did not differ but were both larger than the P1s in young adults. In addition, eFN amplitudes significantly decreased with age. The dissociable distraction patterns between the posterior P1 and eFN provide evidence not only for the timing hypothesis of emotion regulation but also for different developmental trajectories of visual processing areas and the prefrontal cortex during affective processing in adolescence.

. Introduction When experiencing strong emotional responses or when viewing them in others there are a variety of strategies that one can take to reduce the unpleasantness of such responses. The timing hypothesis proposes that emotion regulation strategies can be distinguished by which stage in the emotion-generative process they have their primary impact (Sheppes & Gross, 2010). Distraction shifts attention away from the processing of a primary target stimulus toward the competing stimulus and operates at an early stage (Gross, 1998, Gross and Thompson, 2007 and Thiruchselvam et al., 2011). In contrast, reappraisal involves re-evaluating an emotional event’s underlying meaning and operates at a late stage (Sheppes & Gross, 2010). A recent study using event-related potentials (ERPs) has revealed that distraction influences the elaborate meaning-evaluation of emotional stimuli earlier than reappraisal (Thiruchselvam et al., 2011). However, whether distraction modulates the early stage of affective processing is still unclear. This is the focus of the present study. Recent fMRI studies in adults have identified that distraction reduces activation within emotional processing areas such as the amygdala (Knudsen et al., 2011). In contrast, distraction amplifies activation within attentional control areas such as the medial and dorsolateral prefrontal cortex (Kalisch et al., 2006, Kanske et al., 2010, Knudsen et al., 2011 and McRae et al., 2010). However, these neuroimaging investigations did not reveal changes in the temporal processing of affective information. ERPs have high temporal resolution and are well-suited to capturing rapid neural activity related to emotion regulation. In this study we selected a few visual components to study the temporal process of attentional distraction during emotion regulation. It could determine whether distraction leads to less initial processing of stimuli versus suppressing of later processing. The first positive event, the visual P1 component, begins at approximately 70–90 ms with a peak at approximately 80–150 ms post-stimulus, and putatively originates in the extrastriate visual cortex (Di Russo et al., 2005). The P1 amplitude indexes early sensory processing (Olofsson, Nordin, Sequeira, & Polich, 2008), is sensitive to attention allocation (Brown et al., 2010, Luck et al., 1994 and Smith et al., 2003), and is heightened for emotional stimuli compared to neutral stimuli (Holmes, Nielsen, Tipper, & Green, 2009). Separate from occipital activity (Saron, Schroeder, Foxe, & Vaughan, 2001), the early frontal negativity (eFN) is a broad negative wave over 150–300 ms (overlapping with the N1/P2/N2 complex) (Karayanidis and Michie, 1996, Karayanidis and Michie, 1997, Kurira-Tashima et al., 1992 and Zani and Proverbio, 1995). The eFN is sensitive to attention demands (Karayanidis & Michie, 1997) and is elicited during conflict and inhibition tasks (Nieuwenhuis et al., 2003 and Van Veen and Carter, 2002). In addition, the eFN might reflect an attentional mechanism of the prefrontal cortex, which generates a bias signal that either enhances or suppresses sensory representations in extrastriate visual pathways (Barceló et al., 2000, Hillyard and Anllo-Vento, 1998, Luck et al., 1997 and Pérez-Edgar and Fox, 2003). At the stage of elaborate meaning-evaluation of emotional stimuli, the LPP is a positive-going slow wave that is maximal at central-parietal sites, and begins approximately 300 ms after stimulus onset (Horan et al., 2012, Schupp et al., 2006 and Weinberg et al., 2012). The LPP is sensitive to emotion regulation strategies such as reappraisal and suppression in adults and children (Dennis and Hajcak, 2009, Foti and Hajcak, 2008 and Hajcak and Nieuwenhuis, 2006) as well as affective development in adolescents (Zhang et al., 2012). To date, however, few ERP studies on emotion regulation can be found that apply these components in the study of the development of attentional distraction in adolescents. During adolescence, the adolescent brain continues to mature; it follows a systematic trajectory of frontalization via increased synaptic pruning, continued intra-cortical myelination, and dopaminergic innervation (Rubia et al., 2000), and progressively re-organizes in a back-to-front manner (Yurgelun-Todd, 2007). With age, the prefrontal cortex progressively assumes a greater control over functions that were previously mediated by phylogenetically more primitive structures such as the visual cortices and limbic system (Casey, Getz, & Galvan, 2008). Consistent with these findings, adolescents are better able to allocate attention in accordance with task demands, to resist interference from extraneous stimulation from the environment, and to inhibit inappropriate thoughts and behavioral responses (Segalowitz, Santesso, & Jetha, 2010). However, the level of brain functioning in adolescents is still immature; for example, adolescents tend to demonstrate exaggerated responses to both positive and negative environmental cues compared to adults (Somerville, Jones, & Casey, 2010). The present study examined whether posterior P1 and eFN reflect the developmental changes that occur within the course of attentional distraction during adolescence. We recorded ERPs from 40 adolescent students and 18 undergraduates as they performed a counting task while viewing affective pictures. The emotional intensity of each picture was subsequently rated after performance of the task. Based on the timing hypothesis of emotion regulation (Thiruchselvam et al., 2011), we predicted that the distraction (counting) task would reduce not only the LPP amplitude for positive and negative pictures but also the P1 amplitude for positive and negative pictures relative to simple viewing with no distraction. If the eFN reflects complex attention control of the prefrontal cortex (Nieuwenhuis et al., 2003 and Van Veen and Carter, 2002), then we predicted that counting would enhance the eFN amplitude compared to simple viewing with no distraction. With increasing cortical efficiency less neural processing is necessary to achieve successful performance (Casey et al., 2000 and Rypma, 2007) and therefore we predicted that the P1 and eFN amplitudes would decrease with age.

Results 3.1. Emotional intensity A four-way repeated measures mixed ANOVA yielded a significant main effect of valence on emotional intensity [F(2, 52) = 15.86, p < 0.001, partial η2 = 0.41; Fig. 3a]. Post hoc tests indicated that negative and positive pictures were rated with higher emotional intensity compared to neutral pictures [F(1, 52) = 9.58, p < 0.01, partial η2 = 0.28; F(1, 52) = 9.42, p < 0.01, partial η2 = 0.25, respectively]; however, there was no significant difference between negative and positive pictures [F(1, 52) = 2.42, p > 0.05, partial η2 = 0.06]. A Significant valence × gender interaction [F(2, 52) = 5.42, p < 0.05, partial η2 = 0.18.] indicated that females rated negative pictures as more intense compared to males, but no gender difference was found for positive and neutral pictures. Mean ratings of emotional intensity for positive, neutral, and negative ... Fig. 3. Mean ratings of emotional intensity for positive, neutral, and negative pictures: (a) in the condition of simple viewing with no distraction and counting; (b) among young adolescents, older adolescents, and young adults. The error bars indicate the standard error. *p < 0.05; **p < 0.01. Figure options Moreover, the main effect of the task on emotional intensity reached significance [F(1, 52) = 5.97, p < 0.05, partial η2 = 0.19; Fig. 3a], indicating that counting produced a lower emotional intensity compared to simple viewing with no distraction. In addition, there was a significant main effect of age [F(2, 52) = 10.21, p < 0.01, partial η2 = 0.36; Fig. 3b]. Follow-up analysis indicated that young adolescents rated each picture type as more intense compared to older adolescents and young adults [F(1, 52) = 6.68, p < 0.05, partial η2 = 0.21; F(1, 52) = 6.89, p < 0.05, partial η2 = 0.24, respectively]. No other effects reached statistical significance. 3.2. ERP data 3.2.1. P1 amplitude A four-way repeated measures mixed ANOVA demonstrated that the P1 amplitudes varied as a function of valence [F(2, 52) = 9.64, p < 0.01, partial η2 = 0.26; Fig. 2a], indicating that the P1 amplitudes for negative and positive pictures were more positive compared to neutral pictures [F(1, 52) = 6.51, p < 0.05, partial η2 = 0.21; F(1, 52) = 6.38, p < 0.05, partial η2 = 0.17, respectively]; however, there was no significant difference between positive and negative pictures [F(1, 52) = 2.76, p > 0.05, partial η2 = 0.05]. A Significant valence × gender interaction [F(2, 52) = 5.76, p > 0.05, partial η2 = 0.16] indicated that females showed increased P1 amplitudes for negative pictures compared to males, but no gender difference was found for positive and neutral pictures. We also observed a significant main effect of task, indicating that counting produced lower P1 amplitudes compared to simple viewing with no distraction [F(1, 52) = 8.94, p < 0.01, partial η2 = 0.24; Fig. 2a]. A significant valence × task interaction [F(2, 104) = 6.85, p < 0.01, partial η2 = 0.21] demonstrated that counting reduced P1 amplitudes for negative and positive pictures compared to simple viewing with no distraction [F(1, 52) = 6.57, p < 0.05, partial η2 = 0.18; F(1, 52) = 6.63, p < 0.05, partial η2 = 0.19] but not for neutral pictures [F(1, 52) = 2.49, p > 0.05, partial η2 = 0.04]. The P1 amplitudes varied as a function of age [F(2, 52) = 9.71, p < 0.01, partial η2 = 0.32; Fig. 4]. Post hoc tests indicated that the P1 amplitudes of young and older adolescents were more positive compared to those of young adults [F(1, 52) = 6.53, p < 0.05, partial η2 = 0.17; F(1, 52) = 5.72, p < 0.05, partial η2 = 0.16, respectively]; however, there was no significant difference between young and older adolescents. No other significant effects emerged. Averaged P1 waveforms for positive, neutral, and negative pictures in the ... Fig. 4. Averaged P1 waveforms for positive, neutral, and negative pictures in the condition of simple viewing with no distraction and counting among young adolescents, older adolescents, and young adults. Figure options 3.2.2. eFN A four-way repeated measures mixed ANOVA revealed a significant main effect of valence [F(2, 52) = 14.62, p < 0.001, partial η2 = 0.38; Fig. 2b]. Post hoc tests indicated that negative pictures elicited more negative eFN amplitudes than positive and neutral pictures [F(1, 52) = 8.93, p < 0.01, partial η2 = 0.25; F(1, 52) = 9.35, p < 0.01, partial η2 = 0.30, respectively]; there was no significant difference between positive and neutral pictures [F(1, 52) = 2.92, p > 0.05, partial η2 = 0.05 Fig. 4b]. A significant valence × gender interaction [F(2, 52) = 5.75, p < 0.05, partial η2 = 0.19] indicated that females showed increased eFN amplitudes for positive and negative pictures compared to males, but no gender difference was found for neutral pictures. The four-way ANOVA also showed a significant main effect of task, indicating that counting increased eFN amplitude compared to simple viewing with no distraction [F(1, 52) = 9.86, p < 0.01, partial η2 = 0.31]. Moreover, we also observed a significant valence × task interaction [F(2, 104) = 6.94, p < 0.01, partial η2 = 0.23]. Post hoc tests indicated that compared to simple viewing with no distraction, the counting task increased eFN amplitudes for negative pictures [F(1, 52) = 6.79, p < 0.05, partial η2 = 0.18] but not for positive and neutral pictures [F(1, 52) = 2.81, p > 0.05, partial η2 = 0.04; F(1, 52) = 3.05, p > 0.05, partial η2 = 0.05]. The eFN amplitude varied as a function of age [F(2, 52) = 9.84, p < 0.01, partial η2 = 0.29; Fig. 5]. Post hoc tests indicated that the eFN amplitudes of young adolescents were more negative compared to those of older adolescents and young adults [F(1, 52) = 8.91, p < 0.01, partial η2 = 0.21; F(1, 52) = 9.23, p < 0.01, partial η2 = 0.23, respectively]; eFN amplitudes of older adolescents were also more negative than those of young adults [F(1, 52) = 6.75, p < 0.05, partial η2 = 0.19]. Furthermore, a significant valence × task × age interaction demonstrated that in young adolescents, the eFN amplitude of positive pictures relative to neutral pictures was more negative when counting compared to simple viewing with no distraction [F(4, 208) = 4.61, p < 0.01, partial η2 = 0.19]. No other significant effects emerged. Averaged early frontal negativity (eFN) waveforms for positive, neutral, and ... Fig. 5. Averaged early frontal negativity (eFN) waveforms for positive, neutral, and negative pictures in the condition of simple viewing with no distraction and counting among young adolescents, older adolescents, and young adults. Figure options 3.2.3. LPP Repeated measures mixed ANOVA revealed a significant main effect of valence on the LPP amplitude [F(2, 52) = 9.73, p < 0.01, partial η2 = 0.35; Fig. 2c]. Post hoc tests indicated that the LPP amplitudes for negative and positive pictures were more positive than those for neutral pictures [F(1, 52) = 8.64, p < 0.01, partial η2 = 0.19; F(1, 52) = 8.73, p < 0.01, partial η2 = 0.20, respectively]; however, there was no significant difference between positive and negative pictures [F(1, 52) = 3.06, p > 0.05, partial η2 = 0.05]. A significant valence × gender interaction [F(2, 52) = 5.26, p < 0.05, partial η2 = 0.15] indicated that females showed increased LPP amplitudes for negative pictures compared to males, but no gender difference was found for positive and neutral pictures. We also detected a significant main effect of task, indicating that counting produced lower LPP amplitudes compared to simple viewing with no distraction [F(2, 52) = 10.38, p < 0.01, partial η2 = 0.37; Fig. 2c]. Moreover, a significant task × valence interaction [F(2, 104) = 6.86, p < 0.01, partial η2 = 0.22; Fig. 2a] indicated that compared to simple viewing with no distraction, counting lowered LPP amplitudes for positive and negative pictures [F(1, 52) = 7.53, p < 0.05, partial η2 = 0.19; F(1, 52) = 7.12, p < 0.05, partial η2 = 0.18 Fig. 2a] but not for neutral pictures [F(2, 52) = 2.93, p > 0.01, partial η2 = 0. 05; Fig. 2a]. An age × valence × task interaction [F(4, 208) = 5.06, p < 0.01, partial η2 = 0.26] revealed that compared to simple viewing with no distraction, young adolescents demonstrated a reduced LPP amplitude for negative pictures [F(1, 52) = 6.21, p < 0.05, partial η2 = 0.17] but not for positive pictures [F(1, 52) = 2.43, p > 0.05, partial η2 = 0.04]; however, older adolescents and young adults exhibited reduced LPP amplitudes for negative and positive pictures, while there was no significant LPP amplitude difference among the three groups for neutral pictures. Considering that repetitively performing the same subtraction by 3 would have led to some automaticity in the task, we compared the task effects of the last 10 blocks with those of the first 10 blocks. Counting produced lower LPP amplitudes for the positive and negative pictures in the last 10 blocks compared to the first 10 blocks [F(1, 52) = 5.73, p < 0.05, partial η2 = 0.14; F(1, 52) = 5.86, p < 0.05, partial η2 = 0.15] but not for the neutral pictures [F(1, 52) = 3.05, p > 0.05, partial η2 = 0.05]. 3.3. sLORETA analysis 3.3.1. Source location analysis Because our focus was on early ERP components we chose to source localize only the eFN within 300 ms post-stimulus and not the LPP. Emotional valence identified a significant activation in rostral PFC [BA10; F(2, 52) = 6.79, p < 0.01]. Post hoc tests indicated that the current density during the simple viewing with no distraction was enhanced for negative pictures compared to both positive and neutral pictures (Negative vs. Neutral, p < 0.01; Negative vs. Positive, p < 0.01; Neutral vs. Positive, p > 0.05). As illustrated in Fig. 6, the identified region of the PFC overlaps with the activations identified in fMRI affective processing studies ( Kanske et al., 2010, Knudsen et al., 2011 and McRae et al., 2010). sLORETA analyses revealed that the rostral PFC (BA10) activation within the ... Fig. 6. sLORETA analyses revealed that the rostral PFC (BA10) activation within the early frontal negativity (eFN) window in response to negative pictures was greater compared to both the neutral (a) and positive (b) pictures in the condition of simple viewing with no distraction. Figure options 3.3.2. Current density analysis To assess the task and age effects in emotion-modulated PFC, the average current density in the eFN window in the region-of-interest (ROI) was subjected to valence (positive, neutral, or negative) × task (viewing or counting) × age (between-subject factors: young adolescents, older adolescents, or young adults) repeated measures mixed ANOVA. This analysis revealed significant main effects in valence, task, and age, such that the current density (a) was enhanced for negative pictures compared to positive and neutral pictures [F(2, 52) = 6.63, p < 0.01]; (b) was greater in the counting condition compared to the condition of simple viewing with no distraction [F(1, 52) = 8.67, p < 0.01]; (c) was greater for young adolescents compared to older adolescents and young adults [F(1, 52) = 6.81, 7.14, p < 0.05], and the current density was greater for older adolescents compared to young adults [F(1, 52) = 6.29, p < 0.05]. ANOVA analyses further revealed a significant interaction between valence and task [F(2, 104) = 4.52, p < 0.05]. Post hoc tests revealed a larger activation to negative pictures in the counting condition compared to the condition of simple viewing with no distraction [F(1, 52) = 6.43, p < 0.05] but not for positive and neutral pictures [F(1, 52) = 2.43, 2.61, p > 0.05]. 3.4. Correlation analysis First, Pearson’s correlations between behavioral ratings and ERPs were separately conducted in two task conditions. In the condition of simple viewing with no distraction, behavioral ratings correlated positively with LPP amplitudes (r = 0.37, 0.42, 0.36, all ps < 0.01 for positive, neutral and negative pictures, respectively). In the counting condition, behavioral ratings correlated positively with LPP amplitudes (r = 0.36, 0.40, 0.38, all ps < 0.01 for positive, neutral and negative pictures, respectively), and marginally with eFN amplitudes (r = 0.24, 0.25, 0.23, p = 0.057, 0.068, 054 for positive, neutral and negative pictures, respectively). Second, Pearson’s correlations between counting vs. viewing differences in ERP amplitudes and behavioral ratings were conducted to examine the effect of distraction task on the relationship between behavioral and ERP data. Counting vs. viewing differences in LPP amplitudes correlated positively with behavioral ratings (r = 0.38, 0.45, 0.36, all ps < 0.01 for positive, neutral and negative pictures, respectively). No other correlations reached statistical significance.