International Journal of Psychophysiology 54 (2004) 231 – 240 www.elsevier.com/locate/ijpsycho
Modulation of event-related brain potentials during affective picture processing: a complement to startle reflex and skin conductance response? Christine Amrhein a,b, Andreas Mu¨hlberger c, Paul Pauli c,*, Georg Wiedemann a b
a University Hospital of Psychiatry and Psychotherapy, University of Tu¨bingen, Osianderstr. 24, 72072 Tu¨bingen, Germany Institute of Medical Psychology and Behavioural Neurobiology, University of Tu¨bingen, Gartenstr. 29, 72074 Tu¨bingen, Germany c Institute of Psychology; Biological Psychology, Clinical Psychology and Psychotherapy, University of Wu¨rzburg, Marcusstr. 9 – 11, 97070 Wu¨rzburg, Germany
Received 15 October 2002; received in revised form 1 April 2004; accepted 7 May 2004 Available online 1 July 2004
Abstract The present study compared startle response, skin conductance response (SCR) and subjective variables (valence and arousal ratings, viewing time) assessed in an affective picture paradigm with simultaneously registered event-related brain potentials (ERPs) parameters such as P300 and positive slow waves (PSW). Pleasant, neutral and unpleasant pictures from the International Affective Picture System [Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1999. International Affective Picture System (IAPS): Instruction manual and affective ratings. Technical Report A-4, Center for Research in Psychophysiology. University of Florida, Gainesville, Florida] were presented for 8 s, and startle probes were delivered during picture presentation. Startle response was modulated by picture valence, and SCR by picture arousal. ERP positivity was greater for pleasant and unpleasant than for neutral pictures for the P300 amplitude and the positive slow wave (PSW). ERPs showed characteristic differences and a distinct time course for pictures of different valence categories and may deliver useful information not contained in startle response or SCR measures. The simultaneous registration of startle responses and ERPs in the affective picture paradigm seems valuable. D 2004 Elsevier B.V. All rights reserved. Keywords: Affective picture processing; Event-related potentials; Startle reflex; SCR
1. Introduction Lang et al. (Lang, 1985; Lang et al., 1998) postulated that emotions can be measured on two basic * Corresponding author. Tel.: +49-931-31-2843; fax: +49-93131-2733. E-mail address:
[email protected] (P. Pauli). 0167-8760/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2004.05.009
dimensions: affective valence (from an appetitive to an aversive pole) and arousal. In order to systematically vary emotional valence and arousal during experiments, they have collected a large set of photographic stimuli (International Affective Picture System, IAPS; Lang et al., 1999). In the so-called ‘‘affective picture paradigm’’, these pictures are presented typically for several seconds (6 – 8 s), and subjective as well as physiological responses are
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registered. Covariation between dependent measures and emotional valence and arousal of picture stimuli can be analysed (see Lang et al., 1998, for a review). Psychophysiological variables of interest during affective picture processing have been skin conductance response (SCR) and heart rate (HR) changes. SCR was found to be a reliable indicator of arousal (e.g. Bradley et al., 1993), while HR systematically varies with picture valence (Vrana et al., 1989). Reactions triggered by probe stimuli delivered during picture viewing may also serve as indicators of emotional processing. For example, the startle response triggered by acoustic startle stimuli and quantified by the amplitude of its eye-blink component was found to be increased during viewing of aversive pictures and to be reduced for appetitive pictures (e. g. Vrana et al., 1988; Hamm et al., 1997). However, later studies demonstrated that affective startle modulation is also influenced by arousal, with stronger modulation effects for high- than for low-arousing pleasant and unpleasant stimuli (Schupp et al., 1997; Hamm et al., 1997). Event-related brain potentials (ERPs) have been studied in a variety of cognitive paradigms, but less extensively as indicators of emotional processes. However, they may provide important information about cortical activity evoked by emotional stimuli (e. g. Pauli et al., 1997). Two positive ERP components are of special interest: the P300 (a positive peak occurring approximately 300 ms after stimulus onset) seems to represent attentional processes and processing of new or meaningful stimuli (see Donchin, 1987; Rockstroh et al., 1989, for a review), and the Positive Slow Wave (PSW), which occurs 400 ms after stimulus onset and beyond, and has been found to covary with controlled cognitive processing (Ro¨sler, 1986) and with evaluation and memory storage (Rohrbaugh et al., 1984). There are two approaches to studying the influences of emotional stimuli like IAPS pictures on ERPs. On the one hand, two studies (Schupp et al., 1997; Cuthbert et al., 1998) examined the effects of affective foreground stimuli (IAPS pictures) on the P300 elicited by probe stimuli (startling noises or nonstartling tones). The probe P300 was primarily modulated by picture arousal, with smaller amplitudes elicited when viewing affective (pleasant and unpleasant) as compared to neutral pictures. This reduction of the probe
P300 presumably reflects a greater allocation of attentional resources to affective visual stimuli (Cuthbert et al., 1998). On the other hand, several studies examined ERPs triggered directly by emotional stimuli, adjectives (Naumann et al., 1992), self-selected affective pictures (Johnston et al., 1986; Johnston and Wang, 1991) or IAPS pictures (e. g. Palomba et al., 1997; Keil et al., 2002). These studies found the P300 as well as the PSW to be enhanced for pleasant and unpleasant compared to neutral picture stimuli (Mini et al., 1996; Diedrich et al., 1997; Palomba et al., 1997; Cuthbert et al., 2000; Schupp et al., 2000; Keil et al., 2002). Cuthbert et al. (2000) also found that the PSW was more positive for the higher arousing compared to the lower arousing pictures within each category. Overall, the enhanced late positive components of the ERPs (from about 400 –600 ms on), triggered by emotional stimuli seem to be associated with the arousal dimension and presumably reflect sustained attentive processing of emotionally relevant stimuli (Cuthbert et al., 2000). Finally, some studies (Diedrich et al., 1997; Palomba et al., 1997; Cuthbert et al., 2000) observed an enhanced positivity in an earlier latency range (200 – 300 ms) only for pleasant pictures. This effect was considered to be elicited by picture valence (Diedrich et al., 1997), but it could also be due to other characteristics differing between pleasant and unpleasant pictures. Recent studies (Jungho¨fer et al., 2001; Schupp et al., 2003), however, with brief presentations of affective pictures and multi-channel ERP recordings confirmed the effect of emotional arousal on early ERPs. Besides producing an enhanced late PSW, emotional stimuli also affected early ERP components (as early as 200 ms after picture onset), which can be related to sources of activation in the extended visual system. The early ERP effects presumably reflect facilitated sensory encoding of affective stimuli by early implicit selective attention, while the later ERP effects seem to be related to higher stages of processing (Schupp et al., 2003). In order to understand the significance of ERPs triggered by emotional stimuli, it seems important to simultaneously record other variables — both psychophysiological and self report measures — and to examine their relationship. ERP, startle and peripheral
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responses may complement each other. They reflect different response systems (cortical versus subcortical) which differ in response speed and variability. However, only a few studies have done this systematically. Palomba et al. (1997) measured heart rate and memory performance, and found significant correlations between EEG positivity from 600 to 900 ms and heart rate deceleration, and between P300 amplitude and the number of remembered picture stimuli. Cuthbert et al. (2000) recorded heart rate, skin conductance, corrugator EMG, and valence and arousal ratings. EEG positivity from 400 to 1000 ms loaded on the same factor as SCR and arousal ratings. 1.1. Aims of the present study The present study used an affective picture paradigm to evaluate changes in EEG parameters such as P300 and PSW related to the processing of emotionally pleasant, neutral and unpleasant pictures. PSW was analysed in the latency range from 200 to 2000 ms after picture onset, since this time window seems appropriate to capture both early and late ERP components (see Cuthbert et al., 2000) and was not confounded by startle probes, which were delivered earliest 2.5 s after picture onset. Startle reflex modulation, SCR, viewing time and subjective valence and arousal ratings were also assessed. Since only few studies simultaneously recorded EEG responses and startle reflex modulation, we were especially interested in examining the association between these variables. The aims of the present study were: 1. to replicate the well-known effects (e.g. Lang et al., 1993) of affective pictures on valence and arousal ratings, viewing time, startle reflex magnitude and SCR amplitude; 2. to confirm previous findings (e.g. Cuthbert et al., 2000) that P300 and PSW are enhanced for pleasant and unpleasant pictures compared to neutral ones; 3. to evaluate differences in the time course of the PSW for pleasant, neutral and unpleasant pictures; 4. to demonstrate the concurrent validity of ERPs and startle responses in the affective picture paradigm.
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2. Method 2.1. Participants Sixteen university student volunteers (10 men and 6 women, mean age: 29.5 F 7.9 years) participated in the study. Exclusion criteria were self-reported severe physical illnesses, former or current psychological or psychiatric treatment, and hearing or sight disabilities. Anxiety and psychiatric symptoms were assessed by questionnaires completed after the experiment. Mean values of these questionnaires were comparable to those for other samples of healthy subjects. Participants were advised to avoid alcohol, cigarettes and caffeinated drinks on the day of the experiment. All participants signed an informed consent form and were paid 30 German marks for the 3-h experiment. 2.2. Stimulus material Sixty-six pictures (22 pleasant, 22 neutral, and 22 unpleasant) from the IAPS (Lang et al., 1999) were used; 18 pictures per category served as target stimuli on startle-probed trials1, and four additional pictures in each category were used as filler stimuli and were not used for data evaluation. Five pleasant pictures were different for men and women; they depicted attractive nudes of the opposite sex. The pictures were presented on a 21 inch computer screen at a distance of one meter from the subject’s head. The startlestimulus was a 103 dB, 50 ms burst of white noise with instantaneous rise time. Startle probes were presented binaurally over headphones. 2.3. Procedure and experimental design After having signed an informed consent form, subjects were seated in a comfortable chair in a sound-attenuated room next to the observation room. 1
As target pictures were the same as in the experiment of Bradley et al. (1993). IAPS Picture numbers were as follows: pleasant: for all subjects: 1600, 2080, 2250, 4650, 4660, 4680, 7200, 7330, 7350, 8030, 8080, 8200, 8510; for men: 4180, 4210, 4250 4290, 4310; for women: 4470, 4490, 4500, 4520, 4550; neutral: 2190, 2200, 5500, 7000, 7010, 7020, 7050, 7080, 7090, 7100, 7130, 7150, 7160, 7170, 7180, 7500, 7550, 7700; unpleasant: 1070, 1090, 1120, 1300, 2120, 3000, 3010, 3100, 3130, 3150, 3530, 6020, 6190, 6200, 6230, 6370, 9040, 9490.
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They were instructed that in the first part of the experiment, pictures of different emotional content would be presented on a computer screen, and that each picture should be viewed the entire presentation time. They were also told that at various times during the experiment, they would hear, via headphones, loud noises that could be ignored. To make the participants familiar with the experimental procedure, six sample pictures (two of each picture content, not used in the later experiment) were presented, with a startle probe being delivered during presentation of one picture of each valence category. When subjects indicated that they understood the experimental procedure, the physiological sensors were attached and the participants completed the State-form of the State – Trait – Anxiety Inventory (Spielberger et al., 1970; Spielberger, 1989; German version by Laux et al., 1981). Three startle probes were delivered to avoid startle response outliers during the first trials of picture presentation. In the first part of the experiment, each picture was presented for 8000 ms, with the startle probe being delivered at either 2500, 4000 or 5500 ms after picture onset. The three probe times occurred with equal frequencies for each picture content. Each picture was preceded by a fixation cross appearing in the middle of the screen with a pseudo-randomised duration of 1.5, 2.0, 2.5 or 3.0 s. The time of the fixation cross varied in order to reduce expectations, which would influence the ERP baseline. The inter-trial interval (ITI, blank screen) varied randomly in 2-s increments between 15 and 25 s. To measure the baseline startle reaction, 18 startle probes were presented randomly during ITI (half of them 8 s and half of them 12 s after picture offset). Pictures were arranged such that not more than two pictures of the same picture content and not more than two pictures with the same startle probe presentation time followed each other. For male as well as for female subjects, two different slide presentation orders were designed to vary the serial position of specific pictures and the probe-timing condition for specific pictures and for different ITIs across subjects. After the first part of the experiment, electrodes were removed. Participants were instructed that the pictures would be presented again without startle probes and that they would be able to freely control the viewing time of each picture. After each picture
they were instructed to make subjective ratings for valence and arousal on the Self Assessment Manikin (SAM; Lang, 1980) which was then explained to the subjects. The SAM valence scale shows a graphic figure with expressions ranging from smiling and happy to frowning and unhappy, and the SAM arousal scale shows a figure with expressions ranging from calm and relaxed to excited and wide-eyed. Ratings of valence and arousal are made on nine-point scales. In our version, lower numbers indicate positive valence or higher arousal, and higher numbers indicate negative valence or lower arousal, respectively. Because the standard SAM scales are reversed, we inverted valence and arousal ratings in order to allow comparisons between studies. Both SAM scales were presented on the computer screen, and subjects made their ratings via a computer keyboard. After participants indicated that they understood the procedure, all 54 target pictures were presented again in the same order. At the end of the experiment, subjects completed several questionnaires, and were paid and debriefed. 2.4. Physiological recording and data reduction Startle-responses and skin conductance were registered continuously with a Vitaport-I system (Becker Meditec), and EEG and EOG were recorded continuously with a Synamps amplifier and the software Scan4.1 (Neuroscan). Before attaching the EEG- and startle-electrodes, the skin was cleaned with alcohol and slightly abraded to keep all electrode impedances below 5 kV. The eye-blink component of the startle reflex was measured by recording electromyographic activity from the M. orbicularis oculi muscle beneath the left eye with Ag/AgCl miniature electrodes attached with a constant inter-electrode distance (2.5 cm) across subjects. The raw signal was sampled at 400 Hz, rectified online and integrated with a time constant of 15 ms. Responses to the startle probes were scored manually and defined as EMG peak in a time window from 20 to 250 ms after probe presentation. Trials with excessive baseline shifts or movement artifacts were excluded; trials with no detectable reaction were scored as zero. Startle response magnitudes were then standardized within subjects to correct for the dispro-
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portionate influence of outliers (see Hamm et al., 1997; Globisch et al., 1999). The raw data were first z- and then T-transformed for each subject. Skin conductance was recorded from two electrodes placed on the medial phalanges of the second and third finger of the non-dominant hand. The Vitaport-I system delivered constantly 0.5 V and measured skin conductance with a sampling rate of 400 Hz. SCR elicited by the pictures were scored manually and defined as the largest increase in conductance in a time window from 1.5 to 6.5 s after picture onset. As for startle reflex, trials with artifacts were excluded from analysis, whereas trials with no detectable response were scored as zero. SCR amplitudes were then log-transformed to normalize their distribution. EEG was recorded with Ag/AgCl electrodes from nine sites according to the international 10– 20 system (F3, Fz, F4, C3, Cz, C4, P3, Pz and P4), using a sampling rate of 500 Hz, a bandwidth from 0.15 to 70 Hz and a notch-filter of 50 Hz. The Cz-reference used for recording was converted off-line to a linked mastoid (A1 – A2) reference. Vertical and horizontal eye movements were registered with the same recording parameters as for EEG. Signals were filtered offline with a low pass filter of 15 Hz (12 dB/octave), and trial sweeps from 200 ms before to 2000 ms after picture onset were extracted for further evaluation. EEG was corrected for horizontal and vertical ocular artifacts using the algorithm of Gratton et al. (1983). After baseline correction, segments with remaining artifacts were excluded manually. EEG was then averaged separately for each picture content and electrode site within subjects and recalculated to DC level according to the suggestions of Elbert and Rockstroh (1980). The P300 amplitude was determined as the largest positive peak at Pz in a time window from 300 to 450 ms after picture onset. P300 amplitudes and mean amplitudes of the time windows 200 –300, 300 – 400, 400 –700, 700– 1000, 1000 –1500 and 1500– 2000 ms after picture onset were exported for statistical analyses. These time windows were also used by Cuthbert et al. (2000) and seem appropriate to capture both early and late ERP components. 2.5. Data analysis Valence and arousal ratings, viewing time, startle magnitude and latency, and SCR amplitude and la-
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tency were analysed with repeated measure ANOVAs containing the within-subject factor Picture Content (pleasant, neutral, and unpleasant). The ERP parameters (P300 amplitude and latency, and average amplitude of time windows) were evaluated with ANOVAs containing the within-subject factors Picture Content, Location (frontal, central, parietal) and Laterality (left, middle, right). If necessary, Greenhouse – Geisser corrections of df were applied. Significant Picture Content effects were further analysed with contrasts comparing (1) the neutral with the affective (pleasant and unpleasant) picture categories, and (2) the positive with the negative picture content. Significant Location effects were further analysed by comparing (1) the frontal with the centro-parietal (central and parietal) electrodes, and (2) the central with the parietal electrodes. Significant Laterality effects were further analysed by comparing (1) the midline electrodes with the lateral (left and right) electrodes, and (2) the right with the left electrodes. The startle data of two subjects were excluded from analysis because of few reliable startle responses. The SCRs of one subject were lost due to equipment failure. The EEG data of one subject could not be analysed because of artifacts.
3. Results 3.1. Subjective data, startle reflex and SCR Table 1 provides an overview of the Picture Content mean values for valence and arousal ratings,
Table 1 Means (and SDs) for valence and arousal ratings (scale from 1 to 9), viewing time (in s), startle magnitude (T-transformed; n = 14) and SCR amplitude (log-transformed; n = 15) for pleasant, neutral and unpleasant pictures. Higher valence ratings indicate higher positive affect, and higher arousal ratings indicate higher arousal
Valence ratings Arousal ratings Viewing time Startle magnitude SCR amplitude
Pleasant pictures
Neutral pictures
Unpleasant pictures
6.8 5.0 5.9 48.3 0.42
5.0 (0.3) 2.6 (0.8) 4.7 (3.0) 50.4 (1.5) 0.25 (0.16)
2.7 (0.5) 5.9 (1.0) 4.9 (3.4) 51.3 (1.7) 0.41 (0.22)
(0.5) (1.0) (3.4) (1.5) (0.25)
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viewing time, startle reflex magnitude and SCR. Significant Picture Content effects were found for all three subjective variables: valence ratings [ F(2, 30) = 358.7, p < 0.001], arousal ratings [ F(2, 30) = 151.4, p < 0.001] and viewing time [ F(2, 30) = 6.0, p = 0.009]. Contrast analysis of these Picture Content effects revealed that the valence ratings were higher for the pleasant than for the unpleasant pictures [ F(1,15) = 438.5, p < 0.001] and lower for the neutral pictures compared to affective pictures [ F (1,15) =7.5, p = 0.015]. Arousal ratings were significantly higher for unpleasant than for pleasant pictures [ F(1,15) =16.4, p = 0.001] and significantly lower for neutral than for affective pictures [ F(1,15) =374.2, p <0.001]. Viewing time was significantly longer for pleasant pictures than for unpleasant pictures [ F(1,15) = 6.5, p = 0.022] and for affective compared to neutral pictures [ F(1,15) = 5.3, p = 0.036].
For the startle data, a significant Picture Content effect was found [ F(2, 26) = 8.8, p = 0.001], and contrast analysis revealed that the startle responses for pleasant pictures was significantly smaller than for unpleasant pictures [ F(1,13) = 15.8, p = 0.002]. No differences were found between affective and neutral pictures [ F(1,13) = 0.96, p = 0.35]. The baseline startle response, as measured during ITI, was quite low (47.0 F 2.4), and significantly lower than startle responses during picture viewing (all t’s (13) < 2.7, all p’s < 0.011). Startle latencies did not differ significantly between picture categories. SCR was significantly affected by Picture Content [ F(2, 28) = 12.3, p < 0.001]. A contrast analysis of this effect revealed that the SCR elicited by neutral pictures was significantly smaller than for pleasant or unpleasant pictures [ F(1,14) = 21.4, p < 0.001]. No differences were found between positive and negative pictures [ F(1,14) = 0.04, p = 0.84]. For SCR latencies,
Fig. 1. ERP’s from 100 ms before to 1000 ms after picture presentation for midline and lateral electrodes and the three picture categories; — unpleasant, - - - - neutral, – – pleasant (N = 15).
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no significant differences between picture categories were found. 3.2. EEG data Fig. 1 shows the EEG time course for pleasant, neutral and unpleasant pictures at the three midline and the six lateral electrode sites. The overall EEG waveform (positivity is depicted upwards) showed distinct positive peaks around 200 and 350 ms, and a prominent positive wave beginning at about 400 ms and lasting until about 1000 ms. Table 2 gives an overview of significant ANOVA effects. Significant Picture Content effects were found for the P300 amplitude and for the time windows 200 – 300, 300 – 400, and 400 – 700 ms (marginally significant; p = 0.055). For the remaining time windows and for P300 latency no main or interaction effects involving the factor Picture Content were significant. A significant main effect of Location was found for P300 and for the time windows 300– 400 and 400– 700 ms. Finally, the P300 amplitude was affected by the Location Laterality interaction. No other effects of Laterality or Laterality Location were significant. A further evaluation of the Picture Content effects with planned contrasts (see Table 2) revealed for P300 and for the time windows 200 –300, 300 – 400 and 400 –700 ms an enhanced positivity elicited by affective (pleasant and unpleasant) as compared to neutral pictures. ERPs elicited by positive and negative pic-
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tures did differ (marginally significant p = 0.054) in the time window 200 – 300 ms, with an enhanced positivity for pleasant pictures. Contrasts following the Location effects indicate that the ERP positivity (P300, 300– 400 ms, 400 –700 ms) increased from frontal over central to parietal recording sites.
4. Discussion The aims of this study were to replicate earlier findings on startle reflex and SCR in an affective picture paradigm, and to simultaneously examine ERP differences between pleasant, neutral and unpleasant pictures. The results for subjective parameters, startle reflex and SCR were in accordance with earlier studies (e.g., Greenwald et al., 1989; Vrana et al., 1989). Valence and arousal ratings were comparable to the normative IAPS values (Lang et al., 1999). As hypothesized, startle magnitudes were highest for unpleasant, intermediate for neutral and lowest for pleasant pictures, and SCR was higher for pleasant and unpleasant compared to neutral pictures. Although other studies (e.g. VanOyen Witvliet and Vrana, 2000) reported that startle reflex was also modulated by picture arousal, this was not the case in the present study, as reflected in low startle responses for pleasant pictures. Like previous studies (e.g. Lang et al., 1993; Cuthbert et al., 1996), the present study found significantly longer viewing times for pleasant and unpleas-
Table 2 ANOVA effects and planned contrasts. Significant p-values are printed in bold (df(h,e) = degrees of freedom for hypothesis and error) Factor
df(h,e)
200 – 300 ms
300 – 400 ms
400 – 700 ms
P300
F
p
F
p
F
p
F
p
Picture Content Neutral vs. affective Positive vs. negative Location Frontal vs. centro-parietal Central vs. parietal Laterality Lateral vs. midline Right vs. left Picture Content Location Picture Content Laterality Location Laterality Picture Content Location Laterality
2, 1, 1, 2, 1, 1, 2, 1, 1, 4, 4, 4, 8,
6.3 9.1 4.4 2.4 0.4 5.6 2.0 1.2 2.8 1.3 2.4 1.7 1.5
0.012 0.009 0.054 0.135 0.560 0.033 0.151 0.285 0.119 0.300 0.099 0.195 0.195
5.5 17.2 1.4 8.0 3.5 25.0 3.2 3.8 2.9 0.6 0.7 1.4 0.3
0.016 0.001 0.255 0.010 0.083 0.000 0.060 0.071 0.108 0.606 0.557 0.252 0.896
3.5 11.3 0.1 4.5 2.0 12.9 0.7 1.8 0.1 2.2 1.4 0.3 0.8
0.055 0.005 0.721 0.040 0.181 0.003 0.503 0.197 0.712 0.129 0.250 0.768 0.574
4.9 14.8 0.1 15.1 11.1 34.9 3.0 4.7 2.2 0.2 0.4 3.0 0.5
0.019 0.002 0.757 0.001 0.005 0.000 0.080 0.047 0.160 0.859 0.775 0.045 0.775
28 14 14 28 14 14 28 14 14 56 56 56 112
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ant than for neutral pictures, but in addition an enhanced viewing times for pleasant as compared to unpleasant pictures. This latter finding suggests that viewing time is not directly related to picture arousal and may be influenced by a combination of variables. Cuthbert et al. (1996) proposed that viewing time is affected by picture arousal, subjective interest and, to a lesser degree, by picture valence. EEG findings revealed an enhanced positivity for the P300 and in the time windows 200 –300, 300 – 400, and 400 – 700 ms after picture onset for the affective (pleasant and unpleasant) compared to the neutral pictures. No significant differences were found in the time windows after 700 ms. On the basis of the present and previous studies using IAPS pictures (Diedrich et al., 1997; Palomba et al., 1997; Schupp et al., 2003) we conclude that emotional effects as reflected in ERP become most pronounced from 200 to 700 ms after picture onset. While later ERP effects are presumably related to higher stages of processing, it might be speculated that earlier ERP effects reflect facilitated sensory encoding of affective stimuli by early implicit selective attention (see Schupp et al., 2003). As far as the ERP time course is concerned, most recent studies found a clear arousal modulated EKP response between 200 and 300 ms after stimulus presentation (Schupp et al., 2000, 2003; Keil et al., 2002). However, Diedrich et al. (1997), Palomba et al. (1997), and Cuthbert et al. (2000) reported that early in the picture presentation period, only pleasant pictures evoked a higher positivity than neutral pictures. These findings were partially confirmed in the present study. We found that ERP positivity in the time window 200 –300 ms was higher for pleasant than for unpleasant pictures. Cuthbert et al. (2000) argued that this is an arousal effect because in their study pleasant compared to unpleasant pictures triggered higher SCRs despite of comparable arousal ratings. However, SCRs in our study were comparable for pleasant and unpleasant pictures, and we even found lower arousal ratings for pleasant than for unpleasant pictures. In line with Diedrich et al. (1997) we therefore tentatively interpret this early ERP finding as a valence effect. However, future studies have to systematically disprove alternative explanations (e. g. differences in picture characteristics other than valence).
ERP positivity was generally greatest at parietal electrodes, intermediate at central electrodes, and least at frontal electrodes. Similar to the findings of Cuthbert et al. (2000), Picture Content Effect did not interact with location or laterality. Thus, contrary to hemispheric differences in EEG frequency bands (especially in the alpha band) related to emotional states (e.g. Davidson, 1995; Heller et al., 1997; Pauli et al., 1999; Wiedemann et al., 1999), ERP-related findings do not support the assumption that emotional pictures are processed predominantly in either of the hemispheres. EEG parameters were of special interest in our study because they are more closely linked to cognitive processes than are other psychophysiological variables. Positive ERP components such as P300 and PSW were discussed in the literature as reflecting attentional processes, evaluation of the presented stimuli and memory storage (Rockstroh et al., 1989; Rohrbaugh et al., 1984). Cuthbert et al. (2000) hypothesized that greater positivity for pleasant and unpleasant pictures is due to enhanced attentional processes at encoding for emotionally relevant stimuli. This hypothesis is supported by studies reporting better recall for pleasant and unpleasant as compared to neutral stimuli (e. g. Bradley et al., 1992; Palomba et al., 1997). Enhanced attention, more intense evaluation and better storage of emotionally relevant compared to neutral stimuli may be attributed to underlying motivational factors. According to Lang’s emotion theory (see Lang et al., 1998), pleasant and unpleasant stimuli are especially important for the survival of the individual, and therefore, more strongly activate motivational systems which, in turn, facilitate the processing of these stimuli. One shortcoming of the present study is the rather small sample size, which may have caused a weak statistical power. However, this seems to be unlikely, since the well-established modulations of valence and arousal ratings, SCR, startle response and viewing time within affective stimuli could be replicated, and the ERP findings are also in line with previous reports (Cuthbert et al., 2000; Diedrich et al., 1997). Taken together, the results of our study support the idea that startle reflex is modulated by valence, and SCR is modulated by arousal of emotional picture stimuli. EEG positivity was higher for pleasant and
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unpleasant than for neutral picture stimuli from 200 to 700 ms after picture onset. However, the difference in time course between pleasant and unpleasant pictures speaks against the interpretation of a simple arousal effect. Thus, ERPs seem to complement other psychophysiological variables in the affective picture paradigm, and simultaneous registration of ERPs with startle responses and SCRs was shown to be possible.
Acknowledgements This study was supported by the Deutsche Forschungsgemeinschaft (DFG; Pa 566/3-2).
References Bradley, M.M., Greenwald, M.K., Petry, M., Lang, P.J., 1992. Remembering pictures: pleasure and arousal in memory. J. Exp. Psychol. 18, 379 – 390. Bradley, M.M., Cuthbert, B.N., Lang, P.J., 1993. Pictures as prepulse: attention and emotion in startle modification. Psychophysiology 30, 541 – 545. Cuthbert, B.N., Bradley, M.M., Lang, P.J., 1996. Probing picture perception: activation and emotion. Psychophysiology 33, 103 – 111. Cuthbert, B.N., Schupp, H.T., Bradley, M.M., McManis, M., Lang, P.J., 1998. Probing affective pictures: attended startle and tone probes. Psychophysiology 35, 344 – 347. Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., Lang, P.J., 2000. Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol. Psychol. 52, 95 – 111. Davidson, R.J., 1995. Cerebral asymmetry, emotion, and affective style. In: Davidson, R.J., Hugdahl, K. (Eds.), Brain Asymmetry. MIT Press, Cambridge, MA, pp. 361 – 387. Diedrich, O., Naumann, E., Maier, S., Becker, G., Bartussek, D., 1997. A frontal positive slow wave in the ERP associated with emotional slides. J. Psychophysiol. 11, 71 – 84. Donchin, E., 1987. The P300 as a metric for mental workload. In: Ellingson, R.J., Murray, N.M.F., Halliday, A.M. (Eds.), The London Symposia. Elsevier, Amsterdam, pp. 338 – 343. Elbert, T., Rockstroh, B., 1980. Some remarks on the development of a standarized time constant. Psychophysiology 17, 504 – 505. ¨ hman, A., 1999. Fear Globisch, J., Hamm, A.O., Esteves, F., O appears fast: temporal course of startle reflex potentiation in animal fearful subjects. Psychophysiology 36, 66 – 75. Gratton, G., Coles, M.G., Donchin, E., 1983. A new method for offline removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 55, 468 – 484. Greenwald, M.K., Cook, E.W., Lang, P.J., 1989. Affective judgement and psychophysiological response: dimensional covaria-
239
tion in the evaluation of pictorial stimuli. J. Psychophysiol. 3, 51 – 64. Hamm, A.O., Cuthbert, B.N., Globisch, J., Vaitl, D., 1997. Fear and the startle reflex: blink modulation and autonomic response patterns in animal and mutilation fearful subjects. Psychophysiology 34, 97 – 107. Heller, W., Nitschke, J., Etienne, M., Miller, G., 1997. Patterns of regional brain activity differentiate different types of anxiety. J. Abnorm. Psychology 106, 376 – 385. Johnston, V.S., Wang, X.T., 1991. The relationship between menstrual phase and the P3 component of ERPs. Psychophysiology 28, 400 – 409. Johnston, V.S., Miller, D.R., Burleson, M.H., 1986. Multiple P3s to emotional stimuli and their theoretical significance. Psychophysiology 23 (6), 684 – 694. Jungho¨fer, M., Bradley, M.M., Elbert, T.R., Lang, P.J., 2001. Fleeting images: a new look at early emotion discriminiation. Psychophysiology 38, 175 – 178. Keil, A., Bradley, M.M., Hauk, O., Rockstroh, B., Elbert, T., Lang, P.J., 2002. Large-scale neural correlates of affective picture processing. Psychophysiology 39, 641 – 649. Lang, P.J., 1980. Behavioral treatment and bio-behavioral assessment: computer applications. In: Sidowski, J.B., Johnson, J.H., Williams, T.A. (Eds.), Technology in mental health and delivery systems. Ablex, Norwood, JJ, pp. 119 – 137. Lang, P.J., 1985. The cognitive psychophysiology of emotion: fear and anxiety. In: Tuma, A.H., Maser, J.D. (Eds.), Anxiety and the Anxiety Disorders. Lawrence Erlbaum Associates, Hillsdale, New Jersey, pp. 131 – 170. Lang, P.J., Greenwald, M.K., Bradley, M.M., Hamm, A.O., 1993. Looking at pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology 30, 261 – 273. Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1998. Emotion, attention and the startle reflex. Psychol. Rev. 97 (3), 377 – 395. Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1999. International Affective Picture System (IAPS): Instruction manual and affective ratings. Technical Report A-4, Center for Research in Psychophysiology. University of Florida, Gainesville, Florida. Laux, L., Glanzmann, P., Schaffner, P., Spielberger, C.D., 1981. Das State – Trait – Angstinventar (STAI). Beltz, WeinheimTestgesellschaft. Mini, A., Palomba, D., Angrilli, A., Bravi, S., 1996. Emotional information processing and visual evoked brain potentials. Percept. Mot. Skills 83, 143 – 152. Naumann, E., Bartussek, D., Diedrich, O., Laufer, M.E., 1992. Assessing cognitive and affective information processing functions of the brain by means of the late positive complex of the event-related potential. J. Psychophysiol. 6, 285 – 298. Palomba, D., Angrilli, A., Mini, A., 1997. Visual evoked potentials, heart rate responses and memory to emotional pictorial stimuli. Int. J. Psychophysiol. 27, 55 – 67. Pauli, P., Dengler, W., Wiedemann, G., Montoya, P., Flor, H., Birbaumer, N., Buchkremer, G., 1997. Behavioral and neurophysiological evidence for altered processing of anxiety-related words in panic disorder. J. Abnorm. Psychology 106, 213 – 220. Pauli, P., Wiedemann, G., Nickola, M., 1999. Pain sensitivity, cerebral laterality, and negative affect. Pain 80, 359 – 364.
240
C. Amrhein et al. / International Journal of Psychophysiology 54 (2004) 231–240
Rockstroh, B., Elbert, T., Canavan, A., Lutzenberger, W., Birbaumer, N., 1989. Slow Cortical Potentials and Behaviour, 2nd edn. Urban und Schwarzenberg, Mu¨nchen. Rohrbaugh, J., Newlin, D.B., Varner, J.L., Ellingson, R.J., 1984. Bilateral distribution of the O-wave. In: Karrer, R., Cohen, J., Tueting, P. (Eds.), Brain and Information. Annals of the New York Academy of Sciences, vol. 425. The New York Academy of Sciences, New York, pp. 267 – 270. Ro¨sler, F., 1986. P300 complex: a manifestation of reactive or anticipatory processes of the brain? In: McCallum, W.C., Zapolli, R., Denoth, F. (Eds.), Cerebral Psychophysiology: Studies in EventRelated Potentials. Elsevier, Amsterdam, pp. 138 – 142. Schupp, H.T., Cuthbert, B.N., Bradley, M.M., Birbaumer, N., Lang, P.J., 1997. Probe P3 and blinks: two measures of affective startle modulation. Psychophysiology 34, 1 – 6. Schupp, H.T., Cuthbert, B.N., Bradley, M.M., Cacioppo, J.T., Ito, T., Lang, P.J., 2000. Affective picture processing: the late positive potential is modulated by motivational relevance. Psychophysiology 37, 257 – 261. Schupp, H.T., Jungho¨fer, M., Weike, A.I., Hamm, A.O., 2003. Emotional facilitation of sensory processing in the visual cortex. Psychol. Sci. 14, 7 – 13.
Spielberger, C.D., 1989. State-Trait Anxiety Inventory: A Comprehensive Bibliography, 2nd ed. Consulting Psychologists Press, Palo Alto. Spielberger, C.D., Gorsuch, R.L., Lushene, R.E., 1970. State-Trait Anxiety Inventory (‘‘Self-evaluation questionnaire’’). Consulting Psychologists Press, Palo Alto. VanOyen Witvliet, C., Vrana, S.R., 2000. Emotional imagery, the visual startle, and covariation bias: an affective matching account. Biol. Psychol. 52, 187 – 204. Vrana, S.R., Spence, E.L., Lang, P.J., 1988. The startle-probe response: a new measure of emotion? J. Abnorm. Psychology 97, 487 – 491. Vrana, S.R., Cuthbert, B.N., Lang, P.J., 1989. Processing fearful and neutral sentences: memory and heart rate change. Cogn. Emot. 3, 179 – 195. Wiedemann, G., Pauli, P., Dengler, W., Lutzenberger, W., Birbaumer, N., Buchkremer, G., 1999. Frontal brain asymmetry as a biological substrate of emotions in panic patients. Arch. Gen. Psychiatry 56, 78 – 84.