پاسخ قشری الکترود به احساسات NIMSTIM حالات صورت

Abstract Emotional faces are motivationally salient stimuli that automatically capture attention and rapidly potentiate neural processing. Because of their superior temporal resolution, scalp-recorded event-related potentials (ERPs) are ideal for examining rapid changes in neural activity. Some reports have found larger ERPs for fearful and angry faces compared with both neutral and other emotional faces, and a key aim of the present study was to assess neural response to multiple emotional expressions using the NIMSTIM. Importantly, no study has yet systematically evaluated neural activity and self-report ratings for multiple NIMSTIM expressions. Study 1 examined the time-course of electrocortical activity in response to fearful, angry, sad, happy, and neutral NIMSTIM faces. In Study 2, valence and arousal ratings were collected for the same faces in a separate sample. In line with previous findings, the early P1 was larger for fearful compared with neutral faces. The vertex positivity (VPP) was enhanced for fearful, angry, and happy expressions compared to neutral. There was no effect of expression on the N170. Marginally significant enhancements were observed for all expressions during the early posterior negativity (EPN). The late positive potential (LPP) was enhanced only for fearful and angry faces. All emotional expressions were rated as more arousing and more pleasant/unpleasant than neutral expressions. Overall, findings suggest that angry and fearful faces might be especially potent in terms of eliciting ERP responses and ideal for emotion research when more evocative images cannot be used.

Introduction Decoding facial expressions of emotion is crucial for inferring the states and intentions of others. In this regard, faces might be an especially salient type of emotional stimulus. Indeed, facial expressions of emotion increase cortical arousal and capture attention (Armony and Dolan, 2002, Jiang et al., 2009, Öhman, 2002, Vuilleumier, 2005, West et al., 2009 and Whalen et al., 1998). Because emotional processing tends to be rapid and dynamic, the millisecond resolution of event-related potentials (ERPs) might be ideal for examining neural activity in the context of facial expressions of emotion (e.g., Hajcak et al., 2012). For example, the time-course of neural response to emotional scenes (i.e., International Affective Picture System [IAPS]; Lang et al., 2005) is well documented (Cuthbert et al., 1999, Foti et al., 2009, Keil et al., 2002, Olofsson et al., 2008, Smith et al., 2003 and Weinberg and Hajcak, 2010), and there is evidence that emotional scenes enhance neural processing beginning as early as 100 ms, with sustained increases in neural activity evident for the duration of stimulus presentation (e.g., Hajcak et al., 2010). Taken together, these findings suggest that emotional scenes robustly impact neural activity across multiple processing stages. However, many IAPS pictures include images of mutilated bodies, physical assault, and erotica, which may be inappropriate for certain populations (e.g., children and psychiatric patients). In these instances, stimulus sets using facial expressions of emotion—which have also been shown to potentiate ERPs—might be more appropriate. Indeed, many studies have examined ERPs in response to emotional and neutral faces; however, these studies vary widely in terms of the emotional expressions and stimulus sets employed, as well as the specific ERPs examined. The current study focused on the time-course of neural processing of fearful, angry, happy, sad, and neutral faces using the NIMSTIM facial stimulus set. NIMSTIM is large (i.e., there are more than 600 photos), freely available, full color, and is increasingly-used in studies of emotion (Tottenham et al., 2009). However, no study has systematically assessed ERP responses for multiple NIMSTIM expressions (cf. Blau et al., 2007). In terms of specific ERPs, we evaluated multiple components believed to be sensitive to emotional content (e.g., Eimer and Holmes, 2007): the P1/N1, Vertex Positive Potential (VPP)/N170, Early Posterior Negativity (EPN), and Late Positive Potential (LPP). The P1/N1 complex presents as a positive-going ERP over occipital electrodes, and a negative-going ERP over frontocentral electrodes around 100 ms. The P1 and N1 putatively instantiate early selective attention, and are enhanced for stimuli presented in attended compared to unattended locations (Luck, 1995 and Vogel and Luck, 2000). The P1/N1 is also larger/smaller for emotional compared to neutral scenes (Carretié et al., 2004, Delplanque et al., 2004, Foti et al., 2009, Hot et al., 2006, Keil et al., 2002 and Smith et al., 2003), and the P1/N1 likely originates from regions of occipital and frontal cortex (Carretié et al., 2004, Pessoa and Adolphs, 2010 and Vuilleumier, 2005). However, evidence is less consistent in terms of whether emotional faces modulate the P1 and N1. Some reports observed a greater P1 for unpleasant faces compared to pleasant and neutral faces (i.e., a negativity bias; Bel-Bahar, 2008, Foti et al., 2010, Luo et al., 2010 and Williams et al., 2006), whereas other reports found an enhanced P1 for pleasant and unpleasant faces compared with neutral faces ( Batty and Taylor, 2003 and Esslen et al., 2004). The N1 is relatively understudied in terms of emotional faces. One study observed a more negative N1 for fearful compared to neutral and happy faces ( Luo et al., 2010). Another report found a more negative N1 for neutral compared with fearful faces ( Eimer and Holmes, 2002), and yet another observed no difference between emotional and neutral expressions for the N1 and the P1 ( Eimer et al., 2003). Cross-study discrepancies could be due to variation in task demands (e.g., attention cues, Vogel and Luck, 2000) or stimulus luminosity ( Johannes et al., 1995)—which influence the P1 and N1. Nonetheless, the literature as a whole suggests that under certain circumstances emotional faces can rapidly potentiate sensory and attention processing, and this effect may be especially robust for fearful or angry faces. Following the P1/N1 complex, the VPP is a positive-going ERP maximal over mid-central sites approximately 170 ms after the presentation of faces. Neural processing during the time window of the VPP is enhanced for faces compared with non-faces (Bentin et al., 1996, Sagiv and Bentin, 2001 and Wheatley et al., 2011), and for emotional compared with neutral facial expressions (Ashley et al., 2004, Blau et al., 2007, Eger et al., 2003, Eimer et al., 2003 and Eimer and Holmes, 2007). The VPP also has a lateralized counterpart—the N170—a negative-going ERP that is prominent over occipital-temporal sites when using a nose or average-electrode reference (see Joyce and Rossion, 2005, Fig. 1)1. It has been suggested that the VPP is more sensitive to emotion in faces compared with the N170, and this might result from the VPP being better positioned to reflect contributions from frontal sources (e.g., Eimer and Holmes, 2007, Esslen et al., 2004, Kawasaki et al., 2001 and Williams et al., 2006). Indeed, reports examining the VPP frequently observe enhancement in response to multiple emotional expressions (Ashley et al., 2004, Batty and Taylor, 2003, Eimer et al., 2003, Foti et al., 2010 and Luo et al., 2010), whereas the N170 was not sensitive to emotional content in at least three reports (Ashley et al., 2004, Eimer and Holmes, 2002 and Eimer et al., 2003; cf., Blau et al., 2007). Moreover, similar to the other ERPs discussed herein, the VPP/N170 may be particularly enhanced for fearful or angry faces (Ashley et al., 2004, Batty and Taylor, 2003, Foti et al., 2010 and Vuilleumier, 2005). Overall, the results suggest that processing enhancements in response to facial-affect are particularly evident for the VPP, and fearful expressions may increase processing even more than other emotional expressions. Study 1 participants' (N=41) ERPs time-locked to the onset (0ms) of neutral ... Fig. 1. Study 1 participants' (N = 41) ERPs time-locked to the onset (0 ms) of neutral (gray), fearful (black), angry (red), happy (yellow), and sad (blue) NIMSTIM faces from frontal (top) to occipital (bottom) recording sites. ERPs for Fig. 1 are average-mastoid referenced and negative is plotted upwards. The P1 is apparent at O1/2 at about 100 ms, the N1 at F3/4 around 100 ms, the VPP at C3/4 and CP1/2 at approximately 190 ms, and the LPP appears at CP1/2 beginning around 300 ms. Figure options The Early Posterior Negativity (EPN) follows the VPP/N170 and is a negative-going deflection in the waveform which becomes maximal at temporal-occipital sites between 175 and 275 ms (Foti et al., 2009, Schupp et al., 2006 and Schupp et al., 2003). The EPN is enhanced for emotional compared with neutral stimuli (Foti et al., 2009 and Schupp et al., 2004), including emotional faces (Leppänen et al., 2007, Mühlberger et al., 2009 and Schupp et al., 2004). Emotional enhancement of the EPN putatively indexes enhanced visual processing in the occipital and temporal cortex (Schupp et al., 2003 and Schupp et al., 2006). Moreover, the EPN may be preferentially sensitive to threatening faces (fear and anger) compared with both pleasant and neutral faces (Holmes et al., 2008 and Schupp et al., 2004). As with the N170/VPP, both the EPN and LPP can be observed when using the non-optimal reference scheme, but they emerge more clearly when using the average-electrode or average-mastoid reference, respectively. Moreover, reference choices also impact the emotion enhancement effects on the EPN and LPP: emotional modulation is more prominent when using the optimal reference for a given ERP (Hajcak et al., 2012). The LPP is a positive-going slow wave that is maximal over central-parietal sites around 300 ms. The LPP is associated with sustained attention to motivationally-salient visual scenes (Hajcak et al., 2009, Hajcak et al., 2010, Schupp et al., 2000 and Weinberg and Hajcak, 2011). Importantly, emotional expressions, compared with neutral expressions, also enhance the magnitude of the LPP, suggesting that emotional expressions also cue attention and sustained processing (Eimer et al., 2003, Krolak Salmon et al., 2001 and Luo et al., 2010). However, some studies have observed differential enhancement of the LPP as a function of expression type, with fearful and angry faces eliciting a larger LPP than happy, sad, or neutral faces (Foti et al., 2010, Morel et al., 2009, Schupp et al., 2004 and Williams et al., 2006). Altogether, LPP enhancements are often observed in response to emotional faces, and in some cases, fearful and angry faces may be especially potent in terms of enhancing the LPP (e.g., Eimer et al., 2003, Krolak Salmon et al., 2001, Luo et al., 2010 and Schupp et al., 2004). Altogether, the literature suggests that fearful and angry faces may be especially salient emotional expressions that capture attention and processing resources automatically, similar to emotional scenes containing fearful or threatening images (e.g., Schupp et al., 2004, Vuilleumier, 2005 and Weinberg and Hajcak, 2010). By contrast, processing enhancements for other emotional expressions (i.e., happy, sad) might be less robust, and result from task demands and attention–emotion interactions. For example, passive viewing designs often report increased neural processing across the entire time-course of picture presentation for fearful and angry faces (Eimer and Holmes, 2002, Foti et al., 2010, Schupp et al., 2004 and Williams et al., 2006), whereas emotion discrimination or categorization tasks result in processing enhancements for other emotional expressions (Batty and Taylor, 2003, Bel-Bahar, 2008, Eimer et al., 2003, Krolak Salmon et al., 2001 and Luo et al., 2010). Finally, referencing choices also impact ERP findings, and non-optimal reference schemes can attenuate the effect of emotion on ERPs (Hajcak et al., 2012 and Joyce and Rossion, 2005). In the current study, we utilized a passive viewing paradigm to evaluate the P1/N1, VPP/N170, EPN and LPP in response to angry, sad, happy, fearful, and neutral NIMSTIM faces. A passive viewing design was used to assess which emotional expressions automatically capture attention and enhance neural processing without added task demands. This approach is akin to psychophysiological studies of passively viewed emotional scenes (IAPS; see Bradley et al., 2001, for a review). Given prior reports on face processing and ERPs, we expected all emotional expressions to differ from neutral for the VPP, but fearful and angry expressions were expected to elicit greater processing enhancements than happy, sad, and neutral faces for other ERPs. Study 2 collected arousal and valence self-report ratings to verify that the emotional faces used in Study 1 were perceived as more emotional than neutral, and to record normative valence and arousal ratings for the NIMSTIM set. Although normative ratings exist for angry, fearful, and happy NIMSTIM faces (Adolph and Alpers, 2010 and Blau et al., 2007), self-report ratings have not been collected for sad NIMSTIM expressions, despite their increasing use in studies on depression (e.g., Wisco et al., 2012 and Hankin et al., 2010). Based on previous reports for the NIMSTIM (Adolph and Alpers, 2010 and Blau et al., 2007), and on previous reports for other facial stimulus sets (e.g., Goeleven et al., 2008), all emotional expressions were expected to be rated as more arousing and pleasant/unpleasant than neutral faces.

. Results 3.1. Event-related potentials 3.1.1. Average-mastoid referenced ERPs 3.1.1.1. P1 There was a significant main effect of Expression on the P1 (F(4, 434) = 3.14, p < .05). Pairwise comparisons revealed that only fearful faces elicited a P1 greater than neutral (t(484) = 2.94, p < .01). In fact, fearful faces also cued a larger P1 than angry (t(477) = 2.66, p < .01), happy (t(477) = 2.41, p < .05), and sad (t(472) = 3.13, p < .01) faces. A main effect of Region (F(5, 356) = 58.92, p < .01) revealed that the P1 was greatest over the PO4 electrode. There was no significant Region × Expression interaction (F < 1). 3.1.1.2. N1 The N1 also varied with Expression (F(4, 368) = 2.55, p < .05). The N1 was significantly more negative after the presentation of neutral faces compared to fearful faces (t(406) = 2.46, p < .05); sad faces also elicited a more negative N1 than fearful faces (t(404) = 2.75, p < .01). There was no significant effect of Region, nor Region × Expression interaction (Fs < 1). 3.1.1.3. VPP The VPP differed across Expressions (F(4, 348) = 4.28, p < .01), and pairwise comparisons indicated that fearful (t(401) = 3.34, p < .01), angry (t(406) = 2.62, p < .01), and happy (t(405) = 2.56, p < .05) faces elicited a larger VPP than neutral faces. Sad faces and neutral faces did not significantly differ (t(400) = .30, p > .70). A main of effect of Region indicated that the VPP was maximal over CP1 and CP2 (F(4, 350) = 3.50, p < .01), but there was no significant Region × Emotion interaction (F < 1). 3.1.1.4. LPP There was also a main effect of Expression during the LPP (F(4, 617) = 20.47, p < .01). Fearful (t(624) = 7.32, p < .01) and angry (t(638) = 5.92, p < .01) faces cued a larger LPP than neutral faces. Fearful faces also elicited a larger LPP than happy faces (t(635) = 6.40, p < .01), sad faces (t(641) = 5.80, p < .01), and angry faces (at a trend-level, t(633) = 1.73 p < .10). Happy, sad, and neutral faces cued similar magnitude LPPs (ps > .50). The LPP was greatest at the Pz, P3, and P4 electrodes (main effect of Region; F(7, 400) = 15.05, p < .01), but there was no significant Region × Emotion interaction (F < 1). 3.1.2. Average-electrode referenced ERPs 3.1.2.1. N170 As suggested by Fig. 2, there was no main effect of Expression for the N170 (F < 1). A main effect of Region indicated that the N170 was largest (most negative) at the T7 electrode (F(5, 318) = 92.65, p < .01). The Expression × Region interaction for the N170 was not significant (Fs < 1). 3.1.2.2. EPN There was a marginally significant main effect of Expression on the EPN (F(4, 486) = 1.98. p = .10). Fearful (t(402) = 3.09, p < .01), happy (t(396) = 2.19, p < .05), sad (t(394) = 2.57, p < .05) and angry (t(418) = 2.07, p < .05) expressions elicited a more negative EPN than neutral expressions. The EPN was maximal (most negative) at P7 (F(6, 336) = 75.98, p < 01); there was no significant Expression × Region interaction (F < 1). 3.2. Arousal and valence ratings The descriptive statistics for valence and arousal SAM ratings are presented in Table 2—self-reported arousal differed across Expressions (F(4, 46) = 7.21, p < .01). Pairwise comparisons indicated that fearful (t(38) = 4.21, p < .01), angry (t(40) = 4.29, p < .01), happy (t(35) = 2.41, p < .05), and sad (t(42) = 3.40, p < .01) faces were rated as more arousing than neutral; however, fearful, angry, happy, and sad faces had similar arousal ratings (ps > .25). Results for valence ratings indicated that pleasantness ratings varied with Expression (F(4, 44) = 39.60, p < .01). Post-hoc tests indicated that pleasantness ratings were in expected directions: happy faces were rated as more pleasant than neutral faces (t(26) = 8.10, p < .01), neutral faces were rated more pleasant than sad faces (t(28) = 6.02, p < .01), and there was no difference in pleasantness ratings between sad, angry and fearful faces (ps > .60).