Elsevier

Biological Psychology

Volume 92, Issue 3, March 2013, Pages 447-455
Biological Psychology

The dynamic allocation of attention to emotion: Simultaneous and independent evidence from the late positive potential and steady state visual evoked potentials

https://doi.org/10.1016/j.biopsycho.2011.11.012Get rights and content

Abstract

Emotional stimuli capture and hold attention without explicit instruction. The late positive potential (LPP) component of the event related potential can be used to track motivated attention toward emotional stimuli, and is larger for emotional compared to neutral pictures. In the frequency domain, the steady state visual evoked potential (ssVEP) has also been used to track attention to stimuli flickering at a particular frequency. Like the LPP, the ssVEP is also larger for emotional compared to neutral pictures. Prior work suggests that both the LPP and ssVEP are sensitive to “top-down” manipulations of attention, however the LPP and ssVEP have not previously been examined using the same attentional manipulation in the same participants. In the present study, LPP and ssVEP amplitudes were simultaneously elicited by unpleasant and neutral pictures. Partway through picture presentation, participants’ attention was directed toward an arousing or non-arousing region of unpleasant pictures. In line with prior work, the LPP was reduced when attention was directed toward non-arousing compared to arousing regions of unpleasant pictures; similar results were observed for the ssVEP. Thus, both electrocortical measures index affective salience and are sensitive to directed (here: spatial) attention. Variation in the LPP and ssVEP was unrelated, suggesting that these measures are not redundant with each other and may capture different neurophysiological aspects of affective stimulus processing and attention.

Highlights

► Simultaneously measured the late positive potential (LPP) and the steady state visual evoked potential (ssVEP) to unpleasant and neutral pictures. ► Both the LPP and ssVEP were larger for unpleasant than neutral pictures. ► The LPP and ssVEP were reduced when attention was directed to non-emotional aspects of unpleasant pictures. ► The impact of motivated and directed attention on the LPP and ssVEP were uncorrelated.

Introduction

Attention acts like a focused spotlight that facilitates information processing across multiple cognitive domains; for instance, attention can modulate perception, memory, and action (Luck and Kappenman, 2011). As an example, information presented in attended spatial locations is identified more rapidly and associated with increased early event-related potentials (ERPs) that index facilitated perceptual processing (e.g., an increased N1; Luck and Kappenman, 2011). Like attended information, emotional content is better perceived (Öhman et al., 2001) and remembered (Kensinger and Corkin, 2003) and primes organisms for responsive action (Hajcak et al., 2007). However, individuals do not need to be instructed to attend to emotional content; rather, the facilitated processing of emotional stimuli seems to happen automatically. In other words, the motivational value of environmental stimuli can direct and impact attention – a phenomenon that has been referred to as motivated attention (Lang et al., 1997). Indeed, emotional stimuli elicit larger early ERPs – including the N1 – suggesting increased early selective attention to emotional stimuli (Foti et al., 2009).

Emotional stimuli do not merely capture attention. Rather, evidence suggests visual attention to emotional stimuli is often sustained (Hajcak and Olvet, 2008, Weinberg and Hajcak, 2011b). As long as threat or opportunity is present in the environment, it can benefit from the spotlight of attention. Hajcak and colleagues have argued that the late positive potential (LPP), an electrocortical positivity elicited by emotional and neutral stimuli, can be used to index sustained attention toward motivationally salient stimuli (Hajcak and Olvet, 2008, Weinberg and Hajcak, 2011b). The LPP is maximal at centro-parietal sites as early as 200 ms following stimulus presentation and can last throughout stimulus presentation (Cuthbert et al., 2000, Foti et al., 2010, Hajcak and Olvet, 2008, Schupp et al., 2000). The LPP is larger in response to emotional (i.e., both pleasant and unpleasant) compared to neutral stimuli, including images (Foti et al., 2009, Pastor et al., 2008), words (Fischler and Bradley, 2006, Kissler et al., 2009), and hand gestures (Flaisch et al., 2011). The LPP is larger when stimuli are framed in more negative than neutral terms (Foti and Hajcak, 2008, MacNamara et al., 2009, MacNamara et al., 2011b). Further, the LPP is largest for emotional stimuli that are most directly related to biological imperatives (Briggs and Martin, 2009, Schupp et al., 2004, Weinberg and Hajcak, 2010). For example, pictures that depict erotica and threat elicit the biggest LPPs; on the other hand, exciting sports images are rated as very pleasant and highly arousing, but these images do not elicit particularly large LPPs (Weinberg and Hajcak, 2010).

Although the LPP is sensitive to emotional content, task parameters that reduce attention toward the emotional content of stimuli can attenuate the magnitude of the LPP. For instance, presenting concurrent non-affective tasks that are sufficiently difficult may draw attention away from emotional and neutral pictures, resulting in a reduced LPP (MacNamara et al., 2011a, Sand and Wiens, 2011). In one study, MacNamara et al. (2011a) tested the effect of working memory load on the LPP by having participants memorize either two letters (low-load) or six letters (high-load) followed by the presentation of a neutral or aversive IAPS image during the retention interval. Following picture offset, participants were instructed to recall the letters in the exact order that they appeared. Although the LPP was greater in response to aversive compared to neutral images under low and high working memory load, the overall LPP during high-load was reduced compared to low-load.

Moreover, emotional modulation of the LPP appears to depend on spatial attention. Specifically, when stimuli are presented in spatially unattended areas, or when participants are asked to direct their attention away from arousing picture regions, emotional modulation of the LPP is attenuated (Dunning and Hajcak, 2009, Hajcak et al., 2009, MacNamara and Hajcak, 2009, MacNamara and Hajcak, 2010). For instance, MacNamara and Hajcak (2009) had participants make judgments about whether pairs of neutral or aversive target pictures were the same or different while non-target pictures were simultaneously presented in unattended locations. Affective modulation of the LPP was only apparent when aversive images were presented in attended locations; the aversive pictures in unattended locations did not elicit an increased LPP.

Where attention is allocated within an unpleasant picture also impacts the amplitude of the LPP. Dunning and Hajcak (2009, study 2) used a paradigm in which attention was directed to either more or less arousing areas of emotional images, and examined the impact of this manipulation on the LPP. In this study, participants passively viewed IAPS images for 3000 ms. Following the passive viewing period, a circle appeared over the image directing participants to either an arousing or non-arousing portion of an unpleasant image. The LPP was larger for unpleasant compared to neutral pictures during the passive viewing period; however, in the directed attention period, unpleasant pictures only continued to elicit a larger LPP than neutral pictures when attention was directed to arousing regions. That is, directing attention to non-arousing regions of unpleasant images reduced the amplitude of the LPP (see also Hajcak et al., 2009). Thus, emotional modulation of the LPP critically depends on attention to the emotional content of visually presented stimuli. Moreover, the sustained nature of attention to emotional stimuli is a dynamic process governed both by the motivational properties of stimuli, as well the manner in which organisms intentionally allocate attention.

Whereas the LPP provides information in the time domain about how top-down and bottom-up manipulations of attention influence the processing of emotional stimuli, complementary information in the frequency domain can be obtained using the steady-state visual evoked potentials (ssVEP). The ssVEP is a continuous neural response to stimuli that are repeatedly presented at a rate of approximately 6 Hz or greater, characterized as an oscillatory waveform with the same fundamental frequency as the driving stimulus. Because the driving frequency is known, power in the EEG signal at that frequency can be uniquely attributed to the processing of the flickering stimulus. This measure has been particularly useful in studies of selective attention, in which competing stimuli are presented at different frequencies and ssVEP amplitude at those frequencies is interpreted as reflecting the amount of processing resources devoted to the corresponding stimulus. For example, when spatial attention is manipulated while keeping gaze fixed at a central location, ssVEP amplitude in response to a stimulus in the attended location is increased, regardless of whether that stimulus is task-relevant (Muller et al., 1998) or not (Hillyard et al., 1997, Morgan et al., 1996). Across studies, ssVEP amplitude is generally maximal at posterior sites, and combined EEG and fMRI evidence indicates that it reflects activity in occipital and temporal visual areas (Hillyard et al., 1997). A recent retinotopic mapping study attributed ssVEP amplitude to activity in visual areas V1 and V5/MT, and to a lesser extent V3A, V4, and V8 (Di Russo et al., 2007). Overall, this line of research demonstrates that the ssVEP is an effective tool for examining the effects of attentional manipulations on stimulus processing, representing a reliable measure of activity in both primary and secondary visual cortices.

Complementing this work on selective attention, the ssVEP has also been examined in response to emotional stimuli. Like the LPP, ssVEP amplitude is increased for both pleasant and unpleasant compared to neutral images at parietal and occipital sites (Keil et al., 2003). This finding has also been observed using the steady-state visual evoked field, the magnetic counterpart of the ssVEP (Moratti et al., 2004). In light of this evidence that ssVEP amplitude is sensitive to manipulations of both directed and motivated attention, recent work has begun to examine the interplay between these processes by presenting competing stimuli that vary in emotional content. In one study, participants were required to count geometric patterns presented in one hemifield while ignoring patterns presented in the other hemifield. At the same time, the ssVEP was measured in response to task-irrelevant emotional and neutral images super-imposed over patterns in both hemifields (Keil et al., 2005). Additive effects of spatial attention and emotion were found on the ssVEP, such that the largest ssVEP amplitude was observed for unpleasant images presented in the attended hemifield. By applying Granger causality analysis, a recent study demonstrated that the sustained emotional modulation of ssVEP amplitude is driven in part by re-entrant modulation of activity in visual areas (Keil et al., 2009). Finally, a recent study examined whether individual differences in self-reported social anxiety moderate the ssVEP response to task-irrelevant emotional facial expressions (Wieser et al., 2011). Among individuals high in social anxiety, ssVEP amplitude was increased to angry compared to happy and neutral faces, whereas the ssVEP was not sensitive to the emotional nature of task-irrelevant stimuli for individuals low in social anxiety. As a neural measure that is sensitive to both manipulations of selective attention and the affective content of stimuli, the ssVEP is well-suited for studying interactions between cognition and emotion during visual processing.

The ssVEP and LPP have yet to be considered together in the same study and thus it is unclear whether these measures are related or not. In the current study, we first presented pictures in an uninstructed manner for 3000 ms so that we could assess electrocortical activity elicited by unpleasant and neutral picture content; then, we directed attention to either more or less arousing aspects of unpleasant images for an additional 3000 ms so that we could evaluate the impact of this attentional manipulation on neural activity (Dunning and Hajcak, 2009, study 2; Hajcak et al., 2009). By flickering visual stimuli at 15 Hz, we were able to simultaneously assess the LPP and the ssVEP in both the passive viewing and directed attention portions of each trial. Consistent with our previous work, we predicted that the LPP would be increased when participants passively viewed unpleasant compared to neutral pictures, and that the LPP elicited by unpleasant pictures would be reduced when attention was directed to less emotional aspects of pictures. Insofar as the ssVEP appears similarly sensitive to top-down and bottom-up manipulations of attention, we predicted a similar pattern of results for the ssVEP. Finally, we sought to determine whether these two electrocortical measures of attention – derived from the same data – would be correlated or unique effects.

Section snippets

Participants

Twenty-five undergraduate students (13 female) participated in the current study. The study was approved by the Stony Brook University Institutional Review Board (IRB) and all participants received course credit for their participation.

Stimulus materials

Forty unpleasant pictures (e.g., war scenes, sad faces) and 20 neutral pictures (e.g., buildings, neutral faces) were selected from the International Affective Picture System (IAPS; Lang et al., 2005).1

Results

Fig. 1 depicts the grand average waveforms for the LPP: picture onset occurred at 0 ms; circle onset occurred at 3000 ms and picture offset occurred at 6000 ms. The passive viewing and directed attention windows analyzed are denoted in grey; the distribution of voltage differences on the scalp for unpleasant minus neutral pictures (collapsed across attentional focus) and arousing minus non-arousing focus (collapsed across picture type) are depicted for the passive viewing and directed attention

Discussion

Compared to neutral pictures, unpleasant pictures elicited an increased LPP and increased amplitude of the ssVEP during the passive viewing portion of each trial. These data are consistent with previous work on both the LPP (Cuthbert et al., 2000, Foti et al., 2009, Pastor et al., 2008, Schupp et al., 2000) and ssVEP (Keil et al., 2003, Keil et al., 2005) – both neural measures have been used to index the relatively automatic increase in attention to emotional compared to neutral stimuli.

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