Psychophysiology, 43 (2006), 207–215. Blackwell Publishing Inc. Printed in the USA. Copyright r 2006 Society for Psychophysiological Research DOI: 10.1111/j.1469-8986.2006.00392.x

When does size not matter? Effects of stimulus size on affective modulation

ANDREA DE CESAREI AND MAURIZIO CODISPOTI Department of Psychology, University of Bologna, Bologna, Italy

Abstract Motivationally relevant stimuli have been shown to receive prioritized processing compared to neutral stimuli at distinct processing stages. This effect has been related to the evolutionary importance of rapidly detecting dangers and potential rewards and has been shown to be modulated by the distance between an organism and a faced stimulus. Similarly, recent studies showed degrees of emotional modulation of autonomic responses and subjective arousal ratings depending on stimulus size. In the present study, affective modulation of pictures presented in different sizes was investigated by measuring event-related potentials during a two-choice categorization task. Results showed significant emotional modulation across all sizes at both earlier and later stages of processing. Moreover, affective modulation of earlier processes was reduced in smaller compared to larger sizes, whereas no changes in affective modulation were observed at later stages. Descriptors: Emotion, Attention, Categorization, Stimulus size, ERPs

avoidance when the organism is facing a stimulus that has positive or negative significance, reflecting different behavior according to the distance and the valence of the stimulus. Consistent with the prediction of larger emotional response to nearer stimuli, a study comparing the reaction of snake-phobic participants to snakes presented at various distances (Teghtsoonian & Frost, 1982) showed a linear increase of autonomic responses and self-reported fear as a function of distance. Because distance and retinal size are strictly related (Loftus & Harley, 2005), it can be expected that changes in stimulus size determine arousal modulations similarly to distance. Moreover, in an evolutionary framework, the physical size of an encountered object or organism may determine the motivational relevance for the observer. This possibility is supported by the results of a recent study (Reeves, Lang, Kim, & Tatar, 1999) that investigated autonomic response following arousing and nonarousing stimuli presented in different sizes, suggesting a more pronounced emotional response for bigger compared to smaller stimuli. In the present study, we assessed the possibility that changes in stimulus size may influence the affective modulation of early and late event-related potentials (ERPs). Recently, a number of studies have demonstrated that ERPs may provide useful information regarding early processing of natural emotional stimuli (Jungho¨fer, Bradley, Elbert, & Lang, 2001; Mu¨ller, Keil, Gruber, & Elbert, 1999; Schupp, Jungho¨fer, Weike, & Hamm, 2003, 2004). In particular, a modulation on the basis of stimulus arousal has been observed beginning at around 150 ms poststimulus and lasting approximately 200 ms. Arousing pictures elicit a less pronounced positivity over temporo-occipital areas that is accompanied by a polarity inversion at frontal leads. Although it has been suggested that arousing pictures receive

Although objects may appear under very different viewing conditions (e.g., visual angle, viewing time, orientation, brightness), the human visual system has a remarkable capacity to recognize them and to organize its response adaptively. However, behavior is organized both on the basis of stimulus significance and of contextual cues, which further define the relevance of the stimulus for the observer. In the present study we investigate the hypothesis that the emotional response to biologically relevant stimuli (Bradley, 2000; Lang, Bradley, & Cuthbert, 1997) may vary according to stimulus size. Retinal size is determined both by the physical size of the stimulus and on the distance from the observer, and could play a role in modulating emotional response. In particular, assuming the view that emotions evolved from simpler reactions to biologically relevant threatening or appetitive stimuli, responses to stimuli that are bigger or nearer (e.g., food or an attacking animal) should be particularly pronounced. Both animal studies and human research on phobic and normal individuals described a gradient of behavioral and physiological responses depending on the distance between the organism and the encountered stimulus (Blanchard & Blanchard, 2003; Fanselow, 1994; Lang et al., 1997; Teghtsoonian & Frost, 1982). These patterns of emotional response have been related to the different engagement of the motivational systems depending on the distance from the faced stimulus. Similarly, Miller (1959) described distinct gradients of approach and The authors thank Simone Biondi for his help in data collection. We also thank all the people who volunteered to participate in the study. Address reprint requests to: Maurizio Codispoti, Department of Psychology, University of Bologna, Viale Berti Pichat, 5F40127 Bologna, Italy. E-mail: [email protected]. 207

208 prioritized processing because of their intrinsic relevance (Schupp et al., 2003), neutral stimuli can also result in a similar pattern of activation if they are explicitly made relevant to the task (Codispoti, Ferrari, Jungho¨fer, & Schupp, 2006; Thorpe, Fize, & Marlot, 1996). In target detection paradigms, where one class of stimuli is explicitly made task relevant on the basis of features such as color, spatial frequency, or shape, a less positive ERP is observed over occipital areas (Harter & Aine, 1984; Hillyard & Anllo-Vento, 1998; Mangun, 1995; Ritter, Simson, & Vaughan, 1983). It has been suggested that these effects reflect an early attentional selection process on the basis of stimulus relevance (Hillyard & Anllo-Vento, 1998). Source analysis procedures and brain imaging techniques suggest that generators of this activity are situated in the extrastriate visual cortex. This area is connected via feedforward and feedback connections, both with lower-order visual areas and with other brain structures as the prefrontal cortex and the amygdala. Higher-order structures would exert a top-down control on early visual processing (Bar, 2003; Freedman, Riesenhuber, Poggio, & Miller, 2003; Ghashghaei & Barbas, 2002; Rolls, 2000; Sigala & Logotethis, 2002), prompting the visual system to efficiently respond to relevant stimuli. While early perceptual processes are specific to stimulus modality and rely more on perceptual features, subsequent processing operates on the semantic outcome of categorization processes and should be less influenced by perceptual features. The late positive potential (Kok, 1997, 2001; Ruchkin & Sutton 1983) is a slow positive deflection of the ERP that is observed at centroparietal sensor sites and reflects stages of processing that follow stimulus identification and are modulated by task requirements (Kok, 1997, 2001). Interestingly, when motivationally relevant scenes are presented, a larger late positive potential is observed compared to neutral stimuli (Cacioppo, Crites, Berntson, & Coles, 1993; Cuthbert, Schupp, Bradley, Birbaumer, & Lang, 2000; Schupp et al., 2000). This effect is equally pronounced for pleasant and unpleasant stimuli and has been linked to the concept of motivated attention, which suggests that detection of relevant stimuli may engage attentional resources and activate selective attention processes that further elaborate stimulus contents (Bradley, 2000; Lang et al., 1997). Moreover, affective modulation of the late positive potential covaries with both subjective arousal ratings and autonomic responses (Cuthbert et al., 2000; Lang et al., 1997), reflecting the role of late evaluative processes in regulating patterns of autonomic and behavioral responses. To test the possibility that emotional response may vary according to stimulus size, images differing in emotional content and size were presented to participants, who were asked to categorize them as representing animals or people. Whereas earlier ERP components (e.g., the P1/N1) were expected to vary as a function of perceptual size (Busch, Debener, Kranczioch, Engel, & Herrmann, 2004), ERPs during the 150–300 ms and 400–600 ms time windows were used to assess emotional modulation of picture processing (Cuthbert et al., 2000; Jungho¨fer et al., 2001). Assuming that size reduction determines lower relevance of the scene to the observer, a reduction in affective modulation at both early and late stages of processing was expected for smaller compared to larger images. Alternatively, if stimulus size does not modulate the degree of activation induced by the stimulus, no change in affective modulation at either the early or late time interval was expected. Finally, because size reduction also results in decreased discriminability due to the loss of fine details in the

A. De Cesarei and M. Codispoti scene (Loftus & Harley, 2005), we expected that the earlier time window, reflecting emotional modulation of stages of perceptual analysis, would have been more affected by size reduction compared to the late positive potential, which is thought to reflect processes initiated after stimulus recognition.

Methods Participants Sixteen students (8 women) from the University of Bologna volunteered to participate in the present study and signed an informed consent form. Age ranged from 20 to 29 (average 5 22.7, SD 5 2.27). All participants were right-handed. They were recruited through advertisements and agreed to participate in the present study after having been fully informed about the experimental material and the duration. Materials and Design Two hundred sixty-four color pictures were selected from various sources, including the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 2001), the Internet, and document scanning. Each picture belonged to one of four categories: animals (n 5 132), erotic couples (n 5 44), neutral people (n 5 44), and mutilated people (n 5 44). Pictures in full size covered the whole screen area and subtended a visual angle of 21.231 (horizontal)  16.221 (vertical). Three additional size conditions were created by resizing each picture to 50%, 25%, and 12.5% of the original size, corresponding respectively to horizontal and vertical visual angles of 10.711  8.21 (50%), 5.361  4.11 (25%), and 2.681  2.051 (12.5%). The original height/width ratio was preserved after resizing. In the remainder, each size condition will be labeled as the percentage of original size (100%, 50%, 25%, 12.5%). Stimuli were presented on a 19-in. CRT monitor, at 800  600 resolution and a refresh rate of 155 Hz, controlled by an IBM computer and E-Prime software (Schneider, Eschman, & Zuccolotto, 2002). Images were edited to adjust brightness (defined as average RGB energy) and contrast to the same overall value (respectively 155 and 25 on a scale ranging from 0 to 255). Then, images were pasted at the center of a gray background. Because progressively larger portions of gray background are projected on the retina with decreasing picture size, brightness differences between the background and the picture (e.g., background darker than the picture) could have led to overall brightness changes across sizes. To avoid this potential confounding factor, background brightness was equated to the average brightness of all pictures. The experimental session was divided into eight blocks, to enhance the signal-to-noise ratio of ERPs by increasing the number of trials. Each block consisted of the presentation of the entire 264-image data set. Across blocks, the 264 images were presented in a different order. Within each block, 66 pictures were presented in each size. To prevent participants from recognizing a small picture just because the same image was presented in a bigger size in a previous block, we let each participant see each picture in only one size. Therefore, each image was repeated eight times to a single participant, each time in the same size. Procedure Participants sat in front of the computer monitor, with their head supported by a chin rest. The distance between the eyes and the

Stimulus size and affective modulation monitor was 100 cm. Each block was started by the experimenter, and lasted about 15 min. During each trial, a fixation cross was presented on a gray background for 500 ms. Then the image was displayed for 100 ms, followed by a gray screen which lasted 1000 ms. During this time, participants had to respond as to whether the image represented an animal or a person by pressing one of two mouse buttons with the index finger of the dominant hand. Finally, after a variable delay between 500 and 1500 ms, the next trial began. EEG Recording and Processing EEG was recorded at a sampling rate of 500 Hz and a resolution of 0.12 mV from 59 active sites referenced to Cz using an SA Instrumentation Co. (San Diego, CA) UF-64/72BA amplifier and in-house developed acquisition software. Impedance of each sensor was kept below 10 kO. EEG was on-line filtered from 0.01 to 100 Hz. Eye movements were recorded from two bipolar couples of electrodes, placed, respectively, 1 cm above and below the right eye and 1 cm left and right to the side of the eyes. Ocular signal was recorded with a resolution of 0.24 mVat a sample rate of 500 Hz and was on-line filtered from 0.01 to 100 Hz. Off-line analysis was performed using Emegs (Jungho¨fer & Peyk, 2004) and included removal of eye movements from the EEG signal (Gratton, Coles, & Donchin, 1983), low-pass filtering at 30 Hz, artifact detection, sensor interpolation (Jungho¨fer, Elbert, Tucker, & Rockstroh, 2000) and re-referencing to the average of all channels. Finally, a baseline correction based on the 100 ms prior to stimulus onset was performed. Processed data were averaged according to the factors Category and Size. Only trials where participants correctly categorized stimuli were analyzed. Scoring of ERP Components Averaged waveforms were calculated for each participant and experimental condition. ERPs in the 150–300 ms time window were scored as average at occipito-temporal sensor sites (TP7, TP8, P7/T5, P5, P6, P8/ T6, PO7, PO5, PO3, POz, PO4, PO6, PO8) in the time interval between 150 and 300 ms after stimulus onset. Additional analyses were aimed at detailing amplitude and latency of early affective modulation. Therefore, when a significant difference between either pleasant–neutral or unpleasant–neutral was observed, the corresponding difference waveform was calculated and the negative peak1 between 150 and 300 ms was scored in amplitude and latency. Finally, the onset of early affective modulation was also assessed. With this aim, when a significant effect involving picture content was observed, corresponding waveforms were compared by performing consecutive t tests at each time point on the average of the occipito-temporal sensor group. A sequence of 30 consecutive significant (a 5 .01) t tests, corresponding to a time window of 60 ms, was used as a threshold at which a modulation would be accepted as significant. This approach has been recommended by recent ERP guidelines (Luck, 2005), and allows the determination of the onset of a significant 1 Peaks of P1, N1, and of the differential waveforms in the 150–300 ms time interval were determined by identifying, in each nonflat time interval of interest, the 10 points where the absolute value of the gradient (distance between each point and the following) is minimum. This procedure allows the identification of ERP peaks within the selected interval. Among these values, the most positive (or negative) value was interpreted as the peak of the component of interest and scored in amplitude and latency. This procedure achieves good results in determining peaks, and has the advantage of providing accurate amplitude and latency scores while avoiding problems related to latency shifts and local spurious maxima.

209 difference between experimental conditions. Moreover, it has been successfully employed in recent investigations related to the present study (Rugg, Doyle, & Wells, 1995; Thorpe et al., 1996; VanRullen & Thorpe, 2001). The late positive potential was scored as the average ERP amplitude between 400 and 600 ms at centro-parietal sensor sites (FC3, FC1, FCz, FC2, FC4, C3, C1, Cz, C2, C4, CP3, CP1, CPz, CP2, CP4, P3, P1, Pz, P2, P4, PO3, POz, PO4). Additionally, the P1 and the N1 components were scored in amplitude and latency, respectively, on the peak of the positive and negative component in the time windows between 60 and 100 ms and 90 and 150 ms at occipital sensor sites (O1, Oz, O2). Behavioral Variables Response time and accuracy were collected using E-Prime (Schneider et al., 2002). Analysis of response times was performed only on correct trials. Data Analysis The focus of the present study was to investigate the effects of stimulus size on affective modulation. Animal pictures were added to have an explicit categorization task that could allow the examination of the capability to recognize, in all sizes, the content of the presented stimulus. For clarity, we decided to discard animals from the main analysis reported and to focus on human content stimuli.2 All data (ERPs and behavioral responses) were analyzed with a repeated-measures analysis of variance (ANOVA), with factors Category (3 levels, pleasant, neutral, unpleasant) and Size (4 levels).3,4When a significant main effect or interaction was found, additional tests were carried out to describe the direction of the effects. In particular, pairwise comparisons (pleasant vs. neutral, unpleasant vs. neutral, and pleasant vs. unpleasant) were used to better delineate Category effects, and linear trend analysis was carried out when examining the effects of Size. All ANOVAs were conducted using a multivariate test statistic (Wilks’ lambda) as 2 A preliminary ANOVA with factors Size (4 levels) and Category (2 levels, animals vs. neutral) compared ERPs to animal to neutral pictures. Although more positivity in the 150–300 ms time window was observed for animals compared to neutral stimuli, F(1,15) 5 13.6, po.01, Z2 5 .48, and earlier peaking of the N1 was found for animals compared to neutral stimuli, F(1,15) 5 6.69, po.05, Z2 5 .31, in none of the examined time intervals was a significant interaction of Size and Category observed. No other significant effects were observed in this analysis. Therefore, picture size similarly affected animal and neutral picture processing in early and late time intervals. No other significant effects or interactions with size were observed. 3 A preliminary analysis involving the factors of Category, Size, and Laterality was performed on the amplitudes and latencies of all considered ERP components, on the same regions of interest reported in the Methods section but excluding midline sensors. Peak amplitude of the N1 yielded a significant Laterality  Size interaction, F(3,13) 5 7.04, po.01, Z2 5 .62, showing more pronounced N1 amplitude reduction over left (linear contrast F[1,15] 5 16.26, po.001, Z2 5 .52) compared to right regions (linear contrast F[1,15] 5 9.83, po.05, Z2 5 .40). The late positive potential was more prominent on the right, factor Laterality F(1,15) 5 23.4, po.001, Z2 5 .61. In addition, an almost significant Laterality  Size interaction, F(3,13) 5 3.4, p 5 .05, Z2 5 .44, indicates more pronounced effects of size over left (linear contrast F[1,15] 5 66.13, po.001, Z2 5 .82) compared to the left areas (linear contrast F[1,15] 5 55.53, po.001, Z2 5 .79). No other significant effects or interactions involving factor Laterality were observed. 4 To control for repetition effects, an ANOVA with the factors of Block (8 levels), Category (4 levels), and Size (4 levels) was performed. No significant effects involving the Block factor were found in this analysis.

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Figure 1. Global field power and averaged waveforms from PO8, P2, and O2, in all size conditions.

suggested by Vasey and Thayer (1987), to avoid the inflated type I error rate associated with the univariate ANOVA when the sphericity assumption is not met. For each ANOVA test, we calculated and report the partial eta squared, which reflects the proportion of variance that is accounted for by experimental manipulations. Results Figure 1a illustrates the global field power in all size and category conditions, providing information that is independent of the choice of regions of interest. From left to right, each plot represents a size condition ranging from smallest (12.5%, left end) to largest (100%, right end). Progressively larger amplitude of the global field power was observed as the image was made larger. Moreover, category effects (color lines) were observed at both earlier and later latencies. Focusing on one representative electrode from each region of interest, Figure 1b–d illustrates the combined effects of size and category on specific ERP components. In the 150–300 ms time interval, pleasant pictures appeared to be differentiated from neutral and unpleasant stimuli. Furthermore, this difference appeared more pronounced in larger compared to smaller sizes. Replicating previous findings, the late positive potential was larger for arousing (pleasant and unpleasant) compared to neutral pictures. Interestingly, affective modulation of the late positive potential appeared mainly unaffected by changes in image size. In the following, we report statistical analyses regarding ERP effects in all examined time intervals and behavioral responses. Early Modulation (150–300 ms) Figure 2 illustrates scalp topographies of the early emotional modulation. A broad positivity, more pronounced for neutral and unpleasant compared to pleasant stimuli, is observed over occipito-temporal regions. Analysis of ERP amplitude in the

early time window yielded a significant Category effect, F(2,14) 5 46.68, po.001, Z2 5 .87. However, whereas significant differences between pleasant stimuli versus all other categories were observed, pso.001, no difference between unpleasant and neutral stimuli was found, p>.05. A significant effect of Size was also observed in this time interval, F(3,13) 5 13.73, po.001, Z2 5 .75, characterized by a significant linear trend F(1,15) 5 36.33, po.001, Z2 5 .71, indicating progressively less pronounced positivity for smaller compared to larger stimuli. Furthermore, as illustrated in Figure 2, a significant Size  Category interaction pointed out that affective modulation of early ERP amplitude varied with picture size, F(6,10) 5 5.08, po.05, Z2 5 .75. Following this significant interaction, affective modulation of ERP amplitude in the early time interval was analyzed at each picture size. A significant Category effect was observed in all size conditions, Fs(2,14)>15.98, pso.001, Z2>.70 indicating that, in each size, early ERP amplitude to pleasant stimuli was differentiated from neutral and unpleasant pictures, pso.001, and no affective modulation was observed for unpleasant compared to neutral stimuli. Because only the pleasant–neutral difference reached significance, we decided to focus further analyses on the early affective modulation for pleasant compared to neutral scenes. To detail size effects on early affective modulation, the difference between ERPs elicited by pleasant and neutral stimuli was calculated in each size. Figure 3 illustrates differential waveforms over occipito-temporal sensors (upper panel) and topography of the time course of early affective ERP modulation (lower panel). When stimuli were presented in full size, a negative difference was observed at occipito-temporal leads between about 130 and 300 ms. This effect appeared both reduced in amplitude and delayed with decreasing picture size. A significant effect of Size was observed on the amplitude of the peak of the pleasant–neutral difference wave, F(3,13) 5 9.61, po.001,

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tral difference was also significant, F(3,13) 5 26.84, po.001, Z2 5 .86, linear trend F(1,15) 5 76.90, po.001, Z2 5 .84, showing that the peak of the pleasant–neutral differential was delayed in smaller compared to larger sizes. Finally, the onset of the early affective modulation was also assessed. With this aim, waveforms were compared via consecutive t tests (see Methods). Results showed that the onset of the differentiation between pleasant and neutral stimuli was shifted in latency as a function of size, starting at 136 ms in the 100% size condition, 152 ms in 50%, 166 ms in 25%, and 196 ms in the 12.5% condition (see Figure 3, upper panel).

Figure 2. Scalp maps of activity over posterior areas, in the 150–300 ms time interval, for all sizes and categories.

Z2 5 .69, linear trend F(1,15) 5 29.43, po.001, Z2 5 .66, indicating less negative differential for smaller compared to larger stimuli. Analysis of the latency of the peak of the pleasant–neu-

Late Positive Potential Topographies of the late positive potential are shown in Figure 4. A positive ERP was evident over parietal sensors, which was more positively pronounced for pleasant and unpleasant compared to neutral stimuli. Accordingly, analysis of the amplitude of the late positive potential yielded a significant effect of Category, F(2,14) 5 11.05, po0.001, Z2 5 0.61, indicating more positivity for both pleasant and unpleasant compared to neutral stimuli, pso.001. Additionally, pleasant stimuli elicited more positivity compared to unpleasant pictures, po.05. Stimulus size significantly modulated amplitude of the late positive potential, F(3,13) 5 15.57, po0.001, Z2 5 0.78, linear trend F(1,15) 5 43.13, po.001, Z2 5 .74, eliciting a less pronounced late positive potential for smaller compared to larger stimuli. The interaction Category  Size did not reach significance, F(6,10) 5

Figure 3. Size effects on early pleasant–neutral modulation. The same time scale applies to both waveforms and scalp maps. a: Differential waveforms over occipito-temporal sensor group, in all sizes. Horizontal bars highlight time intervals where a statistically significant differentiation was observed. b: Topographies of the difference of pleasant-neutral over posterior areas, in all sizes.

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A. De Cesarei and M. Codispoti ited a more delayed P1 compared to larger pictures, F(3,13) 5 7.04, po.01, Z2 5 .62, linear trend F(1,15) 5 15.92, po.001, Z2 5 .52. Finally, no interaction between the factors Category and Size was observed on P1 latency. With regard to the N1 component, no main Category effect was observed on peak amplitude. A significant main effect of Size indicated that, with decreasing stimulus size, amplitude of the N1 was reduced, F(3,13) 5 7.6, po.01, Z2 5 .64, linear trend F(1,15) 5 20.96, po.001, Z2 5 .58. No interaction between the factors Category and Size was observed on the amplitude of the N1 component. With regards to N1 latency, no main effect of Category was observed. Instead, a significant effect of the Size factor indicated generally longer N1 peak latencies following presentation of smaller compared to larger stimuli, F(3,13) 5 16.77, po.001, Z2 5 .80, linear trend F(1,15) 5 19.3, po.001, Z2 5 .56. Finally, a significant Category  Size interaction was observed, F(6,10) 5 4.48, po.05, Z2 5 .73, showing earlier peaking of the N1 for pleasant pictures compared to other categories in the 100% size condition, pso.05, and no difference between categories in other sizes.

Figure 4. Scalp maps of activity over centro-parietal areas, in the 400– 600 ms time interval, for all sizes and categories.

2.75, n.s. Consistently, Category effects were significant in all sizes, Fs(2,14)>7.4, pso.01, Z2>.51, indicating more positivity for pleasant and unpleasant compared to neutral stimuli, pso.05. To visually compare size effects on early and late ERP components, Figure 5 reports size effects on affective modulation at both stages. Whereas affective modulation of the early component showed a marked decrease with picture size, emotional effects in the 400–600 ms window appeared stable across all sizes. Additional Analyses: P1/N1 No main effect or interaction of Category and Size was observed on the amplitude of the P1 component. With regards to the latency of the P1 peak, a significant Category effect was observed, F(2,14) 5 9.66, po.01, Z2 5 .58, indicating delayed peak latency for unpleasant compared to pleasant and neutral pictures, pso.05. A main effect of Size indicated that smaller stimuli elic-

Behavioral Responses Mean and standard deviations of response times and accuracy per condition are shown in Table 1. Analysis of response times yielded a significant Category effect, F(2,14) 5 22.88, po.001, Z2 5 .77, indicating faster responses to pleasant stimuli compared to neutral and unpleasant pictures, and slower responses to unpleasant stimuli compared to pleasant and neutrals, all pso.01. A significant effect of Size was also observed, slowing response times as stimuli were made smaller, F(3,13) 5 17.74, po.001, Z2 5 .8, linear trend F(1,15) 5 59.45, po.001, Z2 5 .8. Finally, a significant interaction between Category and Size was observed, F(6,10) 5 3.40, po.05, Z2 5 .67, indicating that the slowing of responses across sizes was more pronounced for negative compared to neutral and pleasant pictures, contrast unpleasant versus neutral and positive across sizes F(1,15) 5 23.78, po.001, Z2 5 .61. Analysis of Accuracy yielded a significant Category effect F(2,14) 5 20.74, po.001, Z2 5 .75, indicating a more accurate performance for pleasant compared to neutral and unpleasant stimuli and more errors for unpleasant stimuli compared to pleasant and neutrals pictures, pso.01. Following size reduction, a significant decrease in accuracy was observed, F(3,13) 5 13.19, po.001, Z2 5 .75, linear trend F(1,15) 5 32.4, po.001, Z2 5 .68. This effect was further characterized by an interaction with Category, F(6,10) 5 6.16, po.01, Z2 5 .79, indicating a more pronounced decrease for unpleasant pictures across sizes, contrast unpleasant versus neutral and positive across sizes F(1,15) 5 29.21, po.001, Z2 5 .66. Discussion

Figure 5. Scatterplot and linear fit of affective modulation in the four sizes, separately for early and late ERP intervals.

In a highly complex environment where potentially threatening and appetitive items are distributed, emotional categorization serves the adaptive function of identifying an object or individual as a predator or a potential reward, and consequently organizing responses. In the present study we assessed the possibility that, similar to distance, stimulus size may also modulate affective processing. Consistent with previous studies, emotional content modulated both early and late ERP components. In particular, pleasant pictures elicited a less pronounced positivity in the 150–300 ms time interval and both pleasant and unpleasant pic-

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Stimulus size and affective modulation Table 1. Means (Standard Deviation) of Response Times (in Milliseconds) and Accuracy (Percentage Correct) for Each Affective Content and Stimulus Size Pleasant

100% 50% 25% 12.5% Total

Neutral

Unpleasant

Total

RTs

Accuracy

RTs

Accuracy

RTs

Accuracy

RTs

Accuracy

572.65 (68.80) 585.61 (64.28) 596.05 (75.02) 622.51 (78.62) 594.2 (72.55)

99 (1.16) 97.8 (1.73) 98.72 (1.37) 97.09 (3.32) 98.15 (2.17)

612.16 (86.94) 620.92 (95.24) 637.4 (113.42) 656.16 (104.30) 631.66 (99.49)

97.51 (2.73) 96.87 (3.31) 96.38 (3.14) 94.1 (5.40) 96.22 (3.92)

613.63 (77.94) 630.42 (96.56) 653.02 (83.68) 701.14 (110.19) 649.55 (96.56)

97.73 (1.95) 94.03 (4.95) 93.61 (3.96) 84.23 (9.06) 92.4 (7.43)

599.48 (78.93) 612.32 (87.00) 628.82 (93.42) 659.94 (101.88) 625.14 (92.80)

98.08 (2.11) 96.23 (3.86) 96.24 (3.63) 91.81 (8.36) 95.59 (5.53)

tures were differentiated from neutral pictures in the 400–600 ms time interval. When stimuli were presented in small size, a reduction and delay in emotional modulation was observed only on the early ERP time interval examined. Although previous studies showed lower arousal ratings for stimuli presented in smaller sizes, in the present study affective modulation of the late positive potential was not decreased following size reduction. It has been suggested that a perceptual processing stage that can be modulated by implicit and explicit stimulus relevance can be reflected in early (150–300 ms) ERP components. Current models on early visual processing suggest that information coming from the retina into primary visual areas V1 and V2 is roughly analyzed and projected to other brain structures such as the prefrontal lobe and the amygdala, which in turn send reentrant feedback that can modulate subsequent activity of the primary and secondary visual areas (Bar, 2003; Bradley et al., 2003; Bu¨chel & Friston, 1997; Rolls, 2000; Stefanacci & Amaral, 2002). However, there are several limitations, for instance, regarding color or fine detail information, in the quality of visual information that can be conveyed at this time. Consequently, this biasing mechanism is particularly likely to be disrupted by a change in discriminability of the scene. Accordingly, when discriminability of the image is reduced, early modulation in the 150– 300 ms latency range is largely reduced, possibly because structures producing top-down control do not receive enough information to bias early visual processing (Goffaux, Gauthier, & Rossion, 2003; Mace´, Thorpe, & Fabre-Thorpe, 2005). Similarly, image complexity has been shown to modulate ERPs in the same latency range (Bradley, 2002; Lo¨w, Lang, & Bradley, 2005). On the other hand, in the present study no decrease in affective modulation of the late positive potential was observed following size reduction. The late positive potential represents the ERP correlate of postperceptual processes linked to stimulus evaluation, and is modulated by attentional and motivational factors (Cuthbert et al., 2000; Keil et al., 2002; Kok, 2001; Ruchkin & Sutton, 1983). Whereas early perceptual processes are aimed at understanding the content of a scene and analyzing incoming information from sensory organs (e.g., the retina), later evaluative processes operate on more semantic representations. At this stage, deployment of attentional resources to motivationally relevant items is not expected to be modulated by perceptual characteristics of the stimulus (cf. Ito & Cacioppo, 2004). However, a less pronounced late positive potential was observed for smaller compared to larger images. This result could relate to either lower arousal or discriminability of smaller images. Previous studies showed lower subjective arousal ratings and less pronounced autonomic responses to pictures presented in smaller compared to larger sizes (Detenber & Reeves, 1996; Reeves et al.,

1999). Because amplitude of the late positive potential covaries both with self-reported arousal and skin conductance level (Cuthbert et al., 2000; Lang et al., 1997), present results could reflect lower arousal of smaller pictures. Alternatively, amplitude change of the late positive potential could relate to lower discriminability of smaller images compared to larger ones. However, a larger late positive potential has been observed following presentation of degraded visual stimuli (Kok, 2001; Kok & DeJong, 1981). Therefore, it seems unlikely that present results reflect changes in stimulus discriminability. As Norman and Bobrow (1975) noted, distinct cognitive processes are sensitive to different manipulations, with some being limited by the quality of perceptual data and others by the amount of allowable resources. In this respect, although similarities between affective modulation occurring during early and late time windows have been repeatedly observed, size manipulation allowed the disentanglement of a first stage of processing that can be modulated on the basis of extrinsic and intrinsic relevance, but that relies on the quality of perceptual input, and a later stage that is sensitive to relevance manipulations but has been shown to be less sensitive to perceptual manipulations. Size reduction is also associated with changes in a number of dimensions. Features such as the distribution of spatial frequencies and number of details vary as pictures are made smaller, leading to an overall greater difficulty in discriminating the content of small pictures (Loftus & Harley, 2005). In the present study, this trend was corroborated by a linear, significant impairment of accuracy and response times for smaller images, which was reflected on both P1 and N1. Similarly, perceptual factors may also explicate the lack of early differentiation between unpleasant and neutral stimuli. In the present study, unpleasant pictures were shown to be the most difficult images to discriminate, and this class of stimuli was more affected by size reduction. In conditions where the time allowed to process a scene is short, more difficult images may take more time to be fully processed. Consistently, at later time intervals (400–600 ms), unpleasant pictures were significantly differentiated from neutral pictures. Consistent with this result, in a recent study (Schupp et al., 2004), less pronounced emotional effects in the 150–300 ms time interval for unpleasant than pleasant pictures were observed. Therefore, although suggesting that discrimination difficulty may be unequally distributed among categories, we remark the need expressed by Schupp and colleagues (2004) for more studies investigating emotional response to stimuli belonging to different categories under different perceptual and attentional conditions. Event-related cortical activity is observed following timelocked events, including image onset and offset. In the present

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study, as pictures were presented for a short presentation time and no transition separated pictures from the subsequent blank screen, the abrupt offset could have elicited a potential that overlapped the picture ERP. However, because all images were presented under the same conditions, the offset potential should not differ from category to category. Moreover, this choice is also associated with two main advantages. First, because the picture vanished very early, participants were unlikely to execute exploratory eye movements to scan pictures presented in maximal size. If this had been the case, eye movements would have differentially contaminated conditions where stimuli were presented in large compared to small size, constituting a potential confounding factor. The second advantage is that, because presentation time was below the time usually indicated as necessary to perform a saccade (about 150 ms), present data could be extended by future studies presenting natural complex pictures in the parafovea (cf. Calvo & Lang, 2005; Keil, Moratti, Sabatinelli, Bradley, & Lang, 2004; Perlman et al., 2005). In the present study, affective modulation was investigated using one specific semantic content for each picture category (pleasant, neutral, and unpleasant), and affective modulation was evaluated by means of cortical responses. Future studies might further examine the effect of picture size on affective modulation using a broader spectrum (heart rate, skin conductance response, startle reflex, corrugator activity) of psychophysiological responses as well as other semantic categories for each valence (e.g., human and animal attack, babies, food, contamination; Bradley, Codispoti, Cuthbert, & Lang, 2001). Moreover, in the present study, pictures represented people either in full view or half view or otherwise only showed body details. Consistently, pictures of close-up subjects (e.g., faces) were displayed in a size that was close to real size, whereas pictures of context (e.g., people in urban or natural environments) were displayed in a size that was smaller than the real size of the person. Although in the present study all pictures were presented in all sizes, therefore preventing effects related to an unbalanced scaling factor, it would be interesting to investigate the role of the scaling factor in modulating affective processing. Based on present results, a straightforward prediction would be that, like image size, the scaling factor could modulate early but not late affective processing.

A final remark concerns the use of pictures of different sizes when investigating emotional modulation. Across different experiments, there is a high variance in the size of pictures, ranging from 5.71  4.61 to 251  18.751 horizontal and vertical degrees of visual angle (Cuthbert et al., 2000; Keil et al., 2004; Kimura, Yoshino, Takahashi, & Nomura, 2004; Pessoa, McKenna, Gutierrez, & Ungerleider, 2002). In spite of the possibility that stimulus size may modulate emotional responses, a systematic investigation of the effects of size on emotional modulation has not been conducted yet. In this respect, in the present study distinct ERP modulations were differently sensitive to size reduction, suggesting that the presentation of stimuli in small sizes could affect specific processes, potentially obscuring emotional effects occurring with larger stimuli. However, to validate present observations with regards to a wider set of stimuli and conditions, more studies varying semantic category and viewing conditions are needed. Moreover, present results were obtained with centrally presented images whose projection lies on the fovea, therefore benefiting from maximal visual acuity. When stimuli are presented in the periphery of the visual field, a further decrease in discriminability occurs, therefore potentially impairing categorization processes (cf. Rousselet, 2005).

Summary Although reductions in emotional modulation were observed at specific processing stages, all emotional effects observed for the largest size were significant even in the 2.681  2.051 presentation condition. This finding is particularly noteworthy and provides evidence of the efficiency of the human visual system in detecting relevant stimuli and allocating resources to their processing, even when they are presented in a degraded form. Interestingly, different affective reactions seem to reflect different processes. Although autonomic responses to emotional pictures, probably reflecting processes related to sensory intake and preparation for action (Codispoti, Ferrari, & Bradley, 2006), are affected by stimulus size (Reeves et al., 1999), stimulus categorization and affective modulation reflected in ERPs seem to suggest that modulation of early processes is more affected by stimulus size compared to later stages of emotional perception.

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(Received October 13, 2005; Accepted February 16, 2006)