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The effect of early attention allocation on location-based attention toward a later threat: An ERP study
Neuroscience Letters 523 (2012) 62–66
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
The effect of early attention allocation on location-based attention toward a later threat: An ERP study Huifang Yang a,b,c , Mengchen Dong a,c , Shuqin Chen a,c , Xifu Zheng a,c,∗ a b c
Center for Studies of Psychological Application, South China Normal University, Guangzhou 510631, China Zhanjiang Normal College, Zhanjiang 524048, China Guangdong Key Laboratory of Mental Health and Recognition Science, Guangzhou 510631, China
h i g h l i g h t s Examined the effect of earlier attention processing on later spatial attention allocation. Initial negative primes influenced subsequent spatial attention allocation. Earlier neutral primes had no effect on later spatial attention allocation.
a r t i c l e
i n f o
Article history: Received 28 March 2012 Received in revised form 28 May 2012 Accepted 18 June 2012 Key words: Attention allocation Priming Dot-probe Event-related potentials (ERPs)
a b s t r a c t The current study investigated the effect of earlier attention processing on later spatial attention allocation using a prime stimulus followed by a dot-probe task. Here we recorded event-related potentials (ERPs) respectively when picture primes and face pairs were displayed at the two successive stages. For negative primes, participants showed smaller amplitudes of negative slow wave (NSW) to initial negative picture primes and greater N1 and smaller P2 amplitudes to subsequent face pairs compared with neutral primes. In addition, participants showed greater amplitudes of NSW to initial neutral picture primes and smaller N1 and greater P2 amplitudes to face pairs in neutral compared with negative prime condition. These results suggest that attention allocation toward an earlier threat influences the attention allocation toward the location of a later threat; and the initial neutral detection does not affect spatial attention allocation toward later face pairs. These findings are interpreted in terms of the theory of limited cognitive resources. © 2012 Elsevier Ireland Ltd. All rights reserved.
Initial threat detection influences processing of subsequently encountered stimuli. Previous research suggests that attention bias disappears in the presence of a negative prime [9]. The mechanisms of biased attention selection have been investigated along spatial or temporal dimensions, but few studies have linked the two [25]. Amir et al. [1] studied spatial and temporal attention processes and showed that an initial selective-attention bias interfered with subsequent processing of non-emotional information. As the measure of electrical activity in the brain is promising as an indicator of mental resources [21], event-related potentials (ERPs) can provide detailed information about the temporal structure of attention allocation. The aim of our study was to examine the effect of earlier attention allocation on spatial attention to later negative stimuli using ERPs.
∗ Corresponding author at: Center for Studies of Psychological Application, South China Normal University, Guangzhou 510631, China. Tel.: +86 13602405510; fax: +86 20 8521 6033. E-mail address: [email protected] (X. Zheng). 0304-3940/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2012.06.042
Priming provides a measure of attention allocation at two temporal stages. Priming refers to the phenomenon whereby presentation of a given stimulus biases or alters subsequent behavior [26]. Accumulating evidence suggests that an affective prime can influence individuals’ subsequent cognition and behavior [18]. The dot-probe task provides a direct measure of spatial allocation of attention to threatening information. In the task, one threat-related (negative face) and one neutral (neutral face) stimulus [7] were shown simultaneously. Participants are asked to respond as fast as possible to the target at the location just occupied by one of the face pair [2]. Response latencies provide a ‘snapshot’ of the distribution of participants’ attention, with faster responses to targets at the attended relative to the unattended location. Attention bias toward threat would be inferred by faster responses to targets replacing negative [7] relative to neutral faces. Along these lines, recent studies have combined the priming paradigm and the dot-probe paradigm to study the effect of early threat detection on subsequent cognition. Garner, Mogg and Bradley used a dot-probe paradigm to examine the impact of priming on attention bias and concluded that initial bias to angry faces
H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
was reduced [8]. In an ERP study, Helfinstein et al. [9] used a dotprobe task to examine changes in attention allocation to threat following a word prime; the results showed that attention bias toward a threatening face was suppressed. In the prime phase (PP), neutral primes elicited higher negative slow wave (NSW) amplitude than negative primes, which may reflect resource allocation [21]. Later, for faces displayed in the dot-probe task phase (DPP), more negative N1 amplitude was found for threat than neutral primes, which may reflect visual attention allocation [10] and visuospatial orienting of attention [5]; and P2 amplitude was greater for neutral than threat primes, which is associated with greater attention bias [19]. Although Helfinstein et al. [9] have investigated the suppression of attention bias in anxious relative to non-anxious participants, it remains unclear, however, what cognitive processes might mediate the modification of attention biases in normative samples. In addition to dealing with non-anxious individuals, the present study used pictures as prime material. Unlike the words used in the study of Helfinstein et al. [9], pictures can have a greater impact [12] than verbal materials. Although pictures are more similar to realworld threats, relatively few studies on the suppression of attention bias have made use of picture stimuli. The current study presented participants with either negative or neutral priming pictures prior to a modified dot-probe task. We hypothesized that an early negative bias would preoccupy some attention resources, influencing attention allocation patterns in the subsequent dot-probe task. 17 healthy right-handed participants (9 females, 8 males) from university took part in this experiment as paid volunteers. Their age ranged from 18 to 23 years (mean = 20.48 years, SD = 1.18). All had normal or corrected to normal vision and had no reported history of neurological illness. Informed consent was obtained from all participants. At the beginning of the experiment, to assess anxiety, the participants completed the trait version of the State-Trait Anxiety Inventory [23]. STAI scores (32.14 ± 7.69) of all participants were within the normal range. Prime stimuli consisted of 32 aversive and 32 neutral pictures from the International Affective Picture System (IAPS) [13]. In accordance with the IAPS scoring, the aversive pictures were significantly more negative in valence than were the neutral pictures [2.26 ± 0.49 vs. 5.00 ± 0.35; t(62) = −36.534, p < 0.001] and also higher in arousal value [6.00 ± 0.65 vs. 3.54 ± 0.62; t(62) = 15.52, p < 0.001]. Dot-probe materials included faces display as cue and white arrow as probe. The faces display consisted of 128 face images (32 male, aversive; 32 male, neutral; 32 female, aversive, 32 female, neutral) from the Chinese Affective Facial Picture System (CAFPS) [16]. The aversive faces were significantly more negative in valence than the neutral faces [2.58 ± 0.3 vs. 4.39 ± 0.15; t(126) = 42.21, p < 0.001] and also higher in arousal value [6.4 ± 1.08 vs. 3.86 ± 0.85; t(126) = 14.76, p < 0.001]. The faces display consisted of two photographs, one of a negative and one of a neutral expression; both
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were of the same gender, and one was placed to the left and the other to the right of a central fixation point. On the computer monitor, the distance between two faces was 11 cm; each face was 11 cm high by 8 cm wide. The white probe arrows were 2 cm tall and 1 cm wide. As shown in Fig. 1, all of the trials began with a fixation cross, which remained at the center of the screen for 500 ms, followed by a priming picture, also at the center of the screen, for 200 ms. After a blank screen lasting 300 ms, the faces were displayed for 500 ms, and were then replaced with the probe, which was a small white arrow in the same location as one of the two faces, pointing up or down. The arrow probe appeared on the location of threatening face in the 50% trials, and appeared on the location of neutral face in the other 50% trials. Participants were required to respond to the orientation of the white arrow by pressing ‘F’ for up and ‘J’ for down as quickly and accurately as possible. The trial ended once the participant pressed a button, or after the probe had remained on the screen for 1100 ms without a response. Each participant completed 16 practice trials followed by two test blocks. Each block included 128 trials, resulting in 256 trials total. The experiment was divided into two blocks. In one block, only aversive priming pictures were presented, whereas in the other, only neutral priming pictures were presented. To avoid emotional interference, the neutral priming block was presented before the aversive priming block. All of the trials in each block were automatically generated and fully randomized by the E-prime program. Before and after the experiment, participants filled out a positive and negative affect schedule (PANAS) [24]. After the aversive experimental session, negative PANAS scores significantly increased [t(16) = −4.44, p < 0.001], whereas positive PANAS scores significantly decreased [t(16) = 6.34, p < 0.001]. However, there were no significant changes in either sub-schedule score after the neutral experimental session. EEGs were recorded with Brain Amp DC amplifiers (bandpass = 0.01–100 Hz, sampling frequency = 500 Hz). Recordings were made from 34 scalp locations: FP1, FP2, F3, F4, F7, F8, FT7, FT8, T7, T8, FC3, FC4, C3, C4, P3, CP3, CP4, P4, P7, P8, O1, O2, Fz, FCz, Cz, CPz, Pz, and Oz. Signals were referenced online to the left mastoid (M1), and then re-referenced offline to the average of the two mastoids. Vertical electrooculogram (VEOG) recording electrodes were positioned above and below the left eye and horizontal EOG (HEOG) recording electrodes were positioned at the outer canthi of both eyes. Impedance was below 5 k for all electrodes. ERPs were computed offline for correct trials that were free of ocular and movement artifacts (>±100 V). Each epoch was 600 ms long, including a 100-ms pre-target interval for baseline correction. Using averaging techniques, separate ERP waveforms were derived time locked to the onset of the picture prime display, the faces display. Within each ERP type, trials were divided into negative-prime and neutral-prime trials to create two distinct ERP waveforms.
Fig. 1. The sequence of events in a trial.
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H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
Fig. 2. Grand mean ERPs elicited by the two types of primes in PP and by face onset in DPP.
For the behavioral results, mean accuracies were 97.47% for correctly identifying the direction of the arrow probe. Incorrect trials were excluded from further analysis. A repeated-measures analysis of variance (ANOVA) for response time was conducted with two factors: prime (negative, neutral) and congruency (target location congruent with the negative face, target location incongruent with the negative face). The ANOVA results revealed a significant effect for prime [F(1, 16) = 39.42, p < 0.001, 2 = 0.71], participants responded faster to the target after a negative prime (535.39 ± 7.14 ms) than after a neutral prime (590.27 ± 21.59 ms). Although the main effect of congruency was not significant [F(1, 16) = 1.23, p = 0.28, 2 = 0.07], the targets replacing negative faces (561.59 ± 18.92 ms) were detected faster than targets replacing neutral faces (564.07 ± 19.13 ms). Bias scores were calculated by subtracting the reaction times for congruent-target trials from those for incongruent-target trials. The bias scores for negative prime (−7.29 ± 4.25) were more negative
and smaller [F(1, 32) = 7.37, p < 0.05] than bias scores for neutral prime (1.82 ± 13.17). Fig. 2(left) shows grand-average ERPs for the two prime types in PP at midline electrodes. A 2 (prime type) by 3 (electrode site: Cz, CPz, and Pz) ANOVA on mean amplitude of the NSW (350–450 ms) showed significant main effects for both prime and electrode site [F(1, 16) = 4.32, p = 0.05, 2 = 0.21; F(3, 48) = 8.82, p < 0.001, 2 = 0.34]. Neutral primes (−3.22 ± 0.53 V) evoked a significantly greater overall NSW amplitude than did negative primes (−1.73 ± 0.87 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to the picture prime is shown in Fig. 3(a), indicating the prominent difference over the posterior scalp regions in this time window. Grand average ERPs in response to face stimuli are presented in the right-hand column of Fig. 2, demonstrating different N1 and P2 amplitudes across the two types of prime conditions.
H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
Fig. 3. Topographies of difference waves formed by subtracting negative trial ERPs from neutral trial ERPs in PP and DPP: (a) 350–450 ms after picture prime; (b) 120–150 ms after face onset; (c) 155–200 ms after face onset.
A 2 (prime type) by 5 (electrode site: Fz, FCz, Cz, CPz, and Pz) ANOVA on N1 (120–150 ms) amplitude showed significant main effect for prime and electrode site [F(1, 16) = 4.91, p < 0.05, 2 = 0.24; F(4, 64) = 2.94, p < 0.05, 2 = 0.16]. N1 mean amplitude was greater and more negative for negative primes (−2.04 ± 0.56 V) than for neutral primes (−0.69 ± 0.75 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to face stimuli is presented in Fig. 3(b), showing the distinct difference over the fronto-central scalp regions in this time window. Similar ANOVAs on P2 (155–200 ms) amplitudes with 5 electrodes (Fz, FCz, Cz, CPz, and Pz) revealed significant effects for prime and electrode site [F(1, 16) = 26.5, p < 0.001, 2 = 0.62; F(4, 64) = 24.24, p < 0.001, 2 = 0.6]. P2 mean amplitude was greater for neutral primes (7.02 ± 0.7 V) than for negative primes (4.48 ± 0.61 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to face stimuli is presented in Fig. 3(c), demonstrating the marked difference over the fronto-central scalp regions in this time window. The present study aimed to investigate the effect of earlier attention processing on later spatial attention allocation by combining the priming and dot-probe paradigms. The results are consistent with previous finding [9] in that negative primes can suppress subjects’ attention bias to subsequent negative stimuli relative to neutral primes. Participants who received negative picture primes showed attention bias in the first PP but did not show biased attention allocation toward negative faces in the second DPP (negative bias scores). On the contrary, when participants were primed with neutral picture primes, they did not show attention bias in the first PP but showed biased attention allocation toward a threatening face in the second DPP (positive bias scores). As indicated in a previous dot-probe study [9], positive bias scores reflect greater allocation of spatial attention to the location of the negative faces, whereas negative scores reflect greater allocation of spatial attention to the location of the neutral faces. In line with the behavioral results and previous findings [11], our ERP results showed that negative primes have a privileged status in the neural processing system, capturing attention and depleting the attention resources that might be available later. Therefore, the negative prime pictures in PP led to reduced resources available for processing negative faces in DPP relative to neutral primes. In PP, participants showed higher amplitudes of NSW in response to neutral primes than negative ones. NSW reflects the balance of inhibitory and excitatory processes within the brain circuit involved in stimulus processing [6,22], and the amplitude of NSW could be related to the construct of resource allocation [21]. The variation of NSW amplitude showed the effectiveness of the priming manipulation, confirming that the participants
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processed the neutral and negative primes differently [3,9]. In accordance with previous studies [20], the results suggested that negative pictures can capture more attention resources and require more neural resources than neutral pictures. The electrophysiological responses in PP indicated the initial privileged access of negative stimuli to attention resources compared with neutral stimuli. Based on capacity theories of attention [14] and the theory of limited cognitive resources [21], we suggest that in the negative prime condition, the emotions induced by the negative picture primes automatically occupied attention resources, and these resources became unavailable [15] for subsequent recognition activity relative to neutral prime condition. In DPP, the amplitudes of N1 and P2 to faces display were affected by the earlier primes. N1 reflects attention to stimuli during relatively early stages of perceptual processing [10]. The amplitudes of N1 are influenced by the degree of visual attention allocated to the stimulus [10] and increase with visuospatial orienting of attention [5]. The P2 component is associated with attention and emotion evaluation [4]. Specifically, in the negative prime condition, participants showed a greater N1 and smaller P2 to faces display, indicating diminished cognitive capacity and processing resources in response to face pairs presented after negative primes. Thus, the smaller P2 may reflect less attention captured by later threat faces due to the depletion of initial attention resources by negative primes, indicating the attention bias disappeared. On the contrary, in the neutral prime condition, decreases in N1 and increases in P2 to face onset were found, reflecting top-down and more elaborate processing of emotional stimuli [4]. Thus, more spatial attention was allocated to negative face and attention bias occurred in DPP after neutral prime. A novel implication of our findings is that negative emotion could influence subsequent spatial attention allocation in normal non-clinical individuals relative to neutral emotion. From a view of evolutionary psychology, our findings may have general implications in the attention processing when encountering a continuous string of stimuli. First, the result that negative pictures can capture our attention resources may provide evidence for the opinion emphasizing the importance of early detection of threat, and the opinion about evolutionary preference for threat stimuli, which has been described as “natural selective attention”. Second, the enhanced processing of initial threat may hinder attention capture by later threat faces, so the usual attention bias was suppressed following the negative prime. Third, unlike previous study [19], our findings indicated that initial threat detection influenced both early visuospatial orienting of attention (N1) and later more elaborated attention processes (P2) in non-anxious individuals. A limitation of our study is the duration of 500 ms of the stimulus presentation interval (also the ISI between cues and probes) in DPP. The somewhat long duration of the ISI (500 ms) between cues and probes may have allowed effects of the cues to extinguish before probes appeared [19]. Thus, it will be important to employ a shorter ISI, such as a duration between 100 and 300 ms [17,19]. Future dot-probe studies will manipulate the stimulus duration to get a more complete view of the selective attention in non-anxious individuals. In conclusion, the results of the present study suggest that the patterns of attention allocation to threat can be altered following an affective prime. These behavioral and ERP data may provide important clues as to how initial threat detection influences subsequent cognition. Hence, early attention allocation can interfere with later spatial allocation of attention to threat.
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H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
Acknowledgments This research was supported by the National Natural Science Foundation of China (30970913), Guangdong Key Laboratory of Mental Health and Recognition Science (South China Normal University). We thank Martin Hutchings for his editing efforts and the professional editors of www.textchek.com, and the two anonymous reviewers for their helpful comments. References
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Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
The effect of early attention allocation on location-based attention toward a later threat: An ERP study Huifang Yang a,b,c , Mengchen Dong a,c , Shuqin Chen a,c , Xifu Zheng a,c,∗ a b c
Center for Studies of Psychological Application, South China Normal University, Guangzhou 510631, China Zhanjiang Normal College, Zhanjiang 524048, China Guangdong Key Laboratory of Mental Health and Recognition Science, Guangzhou 510631, China
h i g h l i g h t s Examined the effect of earlier attention processing on later spatial attention allocation. Initial negative primes influenced subsequent spatial attention allocation. Earlier neutral primes had no effect on later spatial attention allocation.
a r t i c l e
i n f o
Article history: Received 28 March 2012 Received in revised form 28 May 2012 Accepted 18 June 2012 Key words: Attention allocation Priming Dot-probe Event-related potentials (ERPs)
a b s t r a c t The current study investigated the effect of earlier attention processing on later spatial attention allocation using a prime stimulus followed by a dot-probe task. Here we recorded event-related potentials (ERPs) respectively when picture primes and face pairs were displayed at the two successive stages. For negative primes, participants showed smaller amplitudes of negative slow wave (NSW) to initial negative picture primes and greater N1 and smaller P2 amplitudes to subsequent face pairs compared with neutral primes. In addition, participants showed greater amplitudes of NSW to initial neutral picture primes and smaller N1 and greater P2 amplitudes to face pairs in neutral compared with negative prime condition. These results suggest that attention allocation toward an earlier threat influences the attention allocation toward the location of a later threat; and the initial neutral detection does not affect spatial attention allocation toward later face pairs. These findings are interpreted in terms of the theory of limited cognitive resources. © 2012 Elsevier Ireland Ltd. All rights reserved.
Initial threat detection influences processing of subsequently encountered stimuli. Previous research suggests that attention bias disappears in the presence of a negative prime [9]. The mechanisms of biased attention selection have been investigated along spatial or temporal dimensions, but few studies have linked the two [25]. Amir et al. [1] studied spatial and temporal attention processes and showed that an initial selective-attention bias interfered with subsequent processing of non-emotional information. As the measure of electrical activity in the brain is promising as an indicator of mental resources [21], event-related potentials (ERPs) can provide detailed information about the temporal structure of attention allocation. The aim of our study was to examine the effect of earlier attention allocation on spatial attention to later negative stimuli using ERPs.
∗ Corresponding author at: Center for Studies of Psychological Application, South China Normal University, Guangzhou 510631, China. Tel.: +86 13602405510; fax: +86 20 8521 6033. E-mail address: [email protected] (X. Zheng). 0304-3940/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2012.06.042
Priming provides a measure of attention allocation at two temporal stages. Priming refers to the phenomenon whereby presentation of a given stimulus biases or alters subsequent behavior [26]. Accumulating evidence suggests that an affective prime can influence individuals’ subsequent cognition and behavior [18]. The dot-probe task provides a direct measure of spatial allocation of attention to threatening information. In the task, one threat-related (negative face) and one neutral (neutral face) stimulus [7] were shown simultaneously. Participants are asked to respond as fast as possible to the target at the location just occupied by one of the face pair [2]. Response latencies provide a ‘snapshot’ of the distribution of participants’ attention, with faster responses to targets at the attended relative to the unattended location. Attention bias toward threat would be inferred by faster responses to targets replacing negative [7] relative to neutral faces. Along these lines, recent studies have combined the priming paradigm and the dot-probe paradigm to study the effect of early threat detection on subsequent cognition. Garner, Mogg and Bradley used a dot-probe paradigm to examine the impact of priming on attention bias and concluded that initial bias to angry faces
H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
was reduced [8]. In an ERP study, Helfinstein et al. [9] used a dotprobe task to examine changes in attention allocation to threat following a word prime; the results showed that attention bias toward a threatening face was suppressed. In the prime phase (PP), neutral primes elicited higher negative slow wave (NSW) amplitude than negative primes, which may reflect resource allocation [21]. Later, for faces displayed in the dot-probe task phase (DPP), more negative N1 amplitude was found for threat than neutral primes, which may reflect visual attention allocation [10] and visuospatial orienting of attention [5]; and P2 amplitude was greater for neutral than threat primes, which is associated with greater attention bias [19]. Although Helfinstein et al. [9] have investigated the suppression of attention bias in anxious relative to non-anxious participants, it remains unclear, however, what cognitive processes might mediate the modification of attention biases in normative samples. In addition to dealing with non-anxious individuals, the present study used pictures as prime material. Unlike the words used in the study of Helfinstein et al. [9], pictures can have a greater impact [12] than verbal materials. Although pictures are more similar to realworld threats, relatively few studies on the suppression of attention bias have made use of picture stimuli. The current study presented participants with either negative or neutral priming pictures prior to a modified dot-probe task. We hypothesized that an early negative bias would preoccupy some attention resources, influencing attention allocation patterns in the subsequent dot-probe task. 17 healthy right-handed participants (9 females, 8 males) from university took part in this experiment as paid volunteers. Their age ranged from 18 to 23 years (mean = 20.48 years, SD = 1.18). All had normal or corrected to normal vision and had no reported history of neurological illness. Informed consent was obtained from all participants. At the beginning of the experiment, to assess anxiety, the participants completed the trait version of the State-Trait Anxiety Inventory [23]. STAI scores (32.14 ± 7.69) of all participants were within the normal range. Prime stimuli consisted of 32 aversive and 32 neutral pictures from the International Affective Picture System (IAPS) [13]. In accordance with the IAPS scoring, the aversive pictures were significantly more negative in valence than were the neutral pictures [2.26 ± 0.49 vs. 5.00 ± 0.35; t(62) = −36.534, p < 0.001] and also higher in arousal value [6.00 ± 0.65 vs. 3.54 ± 0.62; t(62) = 15.52, p < 0.001]. Dot-probe materials included faces display as cue and white arrow as probe. The faces display consisted of 128 face images (32 male, aversive; 32 male, neutral; 32 female, aversive, 32 female, neutral) from the Chinese Affective Facial Picture System (CAFPS) [16]. The aversive faces were significantly more negative in valence than the neutral faces [2.58 ± 0.3 vs. 4.39 ± 0.15; t(126) = 42.21, p < 0.001] and also higher in arousal value [6.4 ± 1.08 vs. 3.86 ± 0.85; t(126) = 14.76, p < 0.001]. The faces display consisted of two photographs, one of a negative and one of a neutral expression; both
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were of the same gender, and one was placed to the left and the other to the right of a central fixation point. On the computer monitor, the distance between two faces was 11 cm; each face was 11 cm high by 8 cm wide. The white probe arrows were 2 cm tall and 1 cm wide. As shown in Fig. 1, all of the trials began with a fixation cross, which remained at the center of the screen for 500 ms, followed by a priming picture, also at the center of the screen, for 200 ms. After a blank screen lasting 300 ms, the faces were displayed for 500 ms, and were then replaced with the probe, which was a small white arrow in the same location as one of the two faces, pointing up or down. The arrow probe appeared on the location of threatening face in the 50% trials, and appeared on the location of neutral face in the other 50% trials. Participants were required to respond to the orientation of the white arrow by pressing ‘F’ for up and ‘J’ for down as quickly and accurately as possible. The trial ended once the participant pressed a button, or after the probe had remained on the screen for 1100 ms without a response. Each participant completed 16 practice trials followed by two test blocks. Each block included 128 trials, resulting in 256 trials total. The experiment was divided into two blocks. In one block, only aversive priming pictures were presented, whereas in the other, only neutral priming pictures were presented. To avoid emotional interference, the neutral priming block was presented before the aversive priming block. All of the trials in each block were automatically generated and fully randomized by the E-prime program. Before and after the experiment, participants filled out a positive and negative affect schedule (PANAS) [24]. After the aversive experimental session, negative PANAS scores significantly increased [t(16) = −4.44, p < 0.001], whereas positive PANAS scores significantly decreased [t(16) = 6.34, p < 0.001]. However, there were no significant changes in either sub-schedule score after the neutral experimental session. EEGs were recorded with Brain Amp DC amplifiers (bandpass = 0.01–100 Hz, sampling frequency = 500 Hz). Recordings were made from 34 scalp locations: FP1, FP2, F3, F4, F7, F8, FT7, FT8, T7, T8, FC3, FC4, C3, C4, P3, CP3, CP4, P4, P7, P8, O1, O2, Fz, FCz, Cz, CPz, Pz, and Oz. Signals were referenced online to the left mastoid (M1), and then re-referenced offline to the average of the two mastoids. Vertical electrooculogram (VEOG) recording electrodes were positioned above and below the left eye and horizontal EOG (HEOG) recording electrodes were positioned at the outer canthi of both eyes. Impedance was below 5 k for all electrodes. ERPs were computed offline for correct trials that were free of ocular and movement artifacts (>±100 V). Each epoch was 600 ms long, including a 100-ms pre-target interval for baseline correction. Using averaging techniques, separate ERP waveforms were derived time locked to the onset of the picture prime display, the faces display. Within each ERP type, trials were divided into negative-prime and neutral-prime trials to create two distinct ERP waveforms.
Fig. 1. The sequence of events in a trial.
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Fig. 2. Grand mean ERPs elicited by the two types of primes in PP and by face onset in DPP.
For the behavioral results, mean accuracies were 97.47% for correctly identifying the direction of the arrow probe. Incorrect trials were excluded from further analysis. A repeated-measures analysis of variance (ANOVA) for response time was conducted with two factors: prime (negative, neutral) and congruency (target location congruent with the negative face, target location incongruent with the negative face). The ANOVA results revealed a significant effect for prime [F(1, 16) = 39.42, p < 0.001, 2 = 0.71], participants responded faster to the target after a negative prime (535.39 ± 7.14 ms) than after a neutral prime (590.27 ± 21.59 ms). Although the main effect of congruency was not significant [F(1, 16) = 1.23, p = 0.28, 2 = 0.07], the targets replacing negative faces (561.59 ± 18.92 ms) were detected faster than targets replacing neutral faces (564.07 ± 19.13 ms). Bias scores were calculated by subtracting the reaction times for congruent-target trials from those for incongruent-target trials. The bias scores for negative prime (−7.29 ± 4.25) were more negative
and smaller [F(1, 32) = 7.37, p < 0.05] than bias scores for neutral prime (1.82 ± 13.17). Fig. 2(left) shows grand-average ERPs for the two prime types in PP at midline electrodes. A 2 (prime type) by 3 (electrode site: Cz, CPz, and Pz) ANOVA on mean amplitude of the NSW (350–450 ms) showed significant main effects for both prime and electrode site [F(1, 16) = 4.32, p = 0.05, 2 = 0.21; F(3, 48) = 8.82, p < 0.001, 2 = 0.34]. Neutral primes (−3.22 ± 0.53 V) evoked a significantly greater overall NSW amplitude than did negative primes (−1.73 ± 0.87 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to the picture prime is shown in Fig. 3(a), indicating the prominent difference over the posterior scalp regions in this time window. Grand average ERPs in response to face stimuli are presented in the right-hand column of Fig. 2, demonstrating different N1 and P2 amplitudes across the two types of prime conditions.
H. Yang et al. / Neuroscience Letters 523 (2012) 62–66
Fig. 3. Topographies of difference waves formed by subtracting negative trial ERPs from neutral trial ERPs in PP and DPP: (a) 350–450 ms after picture prime; (b) 120–150 ms after face onset; (c) 155–200 ms after face onset.
A 2 (prime type) by 5 (electrode site: Fz, FCz, Cz, CPz, and Pz) ANOVA on N1 (120–150 ms) amplitude showed significant main effect for prime and electrode site [F(1, 16) = 4.91, p < 0.05, 2 = 0.24; F(4, 64) = 2.94, p < 0.05, 2 = 0.16]. N1 mean amplitude was greater and more negative for negative primes (−2.04 ± 0.56 V) than for neutral primes (−0.69 ± 0.75 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to face stimuli is presented in Fig. 3(b), showing the distinct difference over the fronto-central scalp regions in this time window. Similar ANOVAs on P2 (155–200 ms) amplitudes with 5 electrodes (Fz, FCz, Cz, CPz, and Pz) revealed significant effects for prime and electrode site [F(1, 16) = 26.5, p < 0.001, 2 = 0.62; F(4, 64) = 24.24, p < 0.001, 2 = 0.6]. P2 mean amplitude was greater for neutral primes (7.02 ± 0.7 V) than for negative primes (4.48 ± 0.61 V). The topography of difference waves (subtracting negative trials from neutral trials) in response to face stimuli is presented in Fig. 3(c), demonstrating the marked difference over the fronto-central scalp regions in this time window. The present study aimed to investigate the effect of earlier attention processing on later spatial attention allocation by combining the priming and dot-probe paradigms. The results are consistent with previous finding [9] in that negative primes can suppress subjects’ attention bias to subsequent negative stimuli relative to neutral primes. Participants who received negative picture primes showed attention bias in the first PP but did not show biased attention allocation toward negative faces in the second DPP (negative bias scores). On the contrary, when participants were primed with neutral picture primes, they did not show attention bias in the first PP but showed biased attention allocation toward a threatening face in the second DPP (positive bias scores). As indicated in a previous dot-probe study [9], positive bias scores reflect greater allocation of spatial attention to the location of the negative faces, whereas negative scores reflect greater allocation of spatial attention to the location of the neutral faces. In line with the behavioral results and previous findings [11], our ERP results showed that negative primes have a privileged status in the neural processing system, capturing attention and depleting the attention resources that might be available later. Therefore, the negative prime pictures in PP led to reduced resources available for processing negative faces in DPP relative to neutral primes. In PP, participants showed higher amplitudes of NSW in response to neutral primes than negative ones. NSW reflects the balance of inhibitory and excitatory processes within the brain circuit involved in stimulus processing [6,22], and the amplitude of NSW could be related to the construct of resource allocation [21]. The variation of NSW amplitude showed the effectiveness of the priming manipulation, confirming that the participants
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processed the neutral and negative primes differently [3,9]. In accordance with previous studies [20], the results suggested that negative pictures can capture more attention resources and require more neural resources than neutral pictures. The electrophysiological responses in PP indicated the initial privileged access of negative stimuli to attention resources compared with neutral stimuli. Based on capacity theories of attention [14] and the theory of limited cognitive resources [21], we suggest that in the negative prime condition, the emotions induced by the negative picture primes automatically occupied attention resources, and these resources became unavailable [15] for subsequent recognition activity relative to neutral prime condition. In DPP, the amplitudes of N1 and P2 to faces display were affected by the earlier primes. N1 reflects attention to stimuli during relatively early stages of perceptual processing [10]. The amplitudes of N1 are influenced by the degree of visual attention allocated to the stimulus [10] and increase with visuospatial orienting of attention [5]. The P2 component is associated with attention and emotion evaluation [4]. Specifically, in the negative prime condition, participants showed a greater N1 and smaller P2 to faces display, indicating diminished cognitive capacity and processing resources in response to face pairs presented after negative primes. Thus, the smaller P2 may reflect less attention captured by later threat faces due to the depletion of initial attention resources by negative primes, indicating the attention bias disappeared. On the contrary, in the neutral prime condition, decreases in N1 and increases in P2 to face onset were found, reflecting top-down and more elaborate processing of emotional stimuli [4]. Thus, more spatial attention was allocated to negative face and attention bias occurred in DPP after neutral prime. A novel implication of our findings is that negative emotion could influence subsequent spatial attention allocation in normal non-clinical individuals relative to neutral emotion. From a view of evolutionary psychology, our findings may have general implications in the attention processing when encountering a continuous string of stimuli. First, the result that negative pictures can capture our attention resources may provide evidence for the opinion emphasizing the importance of early detection of threat, and the opinion about evolutionary preference for threat stimuli, which has been described as “natural selective attention”. Second, the enhanced processing of initial threat may hinder attention capture by later threat faces, so the usual attention bias was suppressed following the negative prime. Third, unlike previous study [19], our findings indicated that initial threat detection influenced both early visuospatial orienting of attention (N1) and later more elaborated attention processes (P2) in non-anxious individuals. A limitation of our study is the duration of 500 ms of the stimulus presentation interval (also the ISI between cues and probes) in DPP. The somewhat long duration of the ISI (500 ms) between cues and probes may have allowed effects of the cues to extinguish before probes appeared [19]. Thus, it will be important to employ a shorter ISI, such as a duration between 100 and 300 ms [17,19]. Future dot-probe studies will manipulate the stimulus duration to get a more complete view of the selective attention in non-anxious individuals. In conclusion, the results of the present study suggest that the patterns of attention allocation to threat can be altered following an affective prime. These behavioral and ERP data may provide important clues as to how initial threat detection influences subsequent cognition. Hence, early attention allocation can interfere with later spatial allocation of attention to threat.
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Acknowledgments This research was supported by the National Natural Science Foundation of China (30970913), Guangdong Key Laboratory of Mental Health and Recognition Science (South China Normal University). We thank Martin Hutchings for his editing efforts and the professional editors of www.textchek.com, and the two anonymous reviewers for their helpful comments. References
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