Motivated and controlled attention to emotion: Time-course of the late positive potential

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Abstract

Objective

The present study examined the time-course of automatic and controlled modulation of the late positive potential (LPP) during emotional picture viewing.

Methods

Participants (N = 32) viewed neutral and unpleasant stimuli for 6000 ms; at 3000 ms, one of two tones signaled participants to attend either to a more or less arousing portion of the picture. The time-course of the LPP was examined both during the passive viewing and directed attention portions of the trial using the method proposed by Guthrie and Buchwald [Guthrie D, Buchwald JS. Significance testing of difference potentials. Psychophysiology 1991;28(2):240–4].

Results

During passive viewing, the LPP became reliably larger following the presentation of unpleasant pictures from 160 ms onward; the magnitude of the LPP became reliably smaller beginning 620 ms after participants were instructed to attend to the less arousing aspects of unpleasant pictures – and this difference was maintained throughout the duration of the trial.

Conclusions

The LPP reflects relatively automatic attention to emotional visual stimuli, but is also sensitive to manipulations of directed attention toward arousing versus neutral aspects of such stimuli.

Significance

These results shed further light on the time-course of emotional and cognitive modulation of the LPP, and suggest that the LPP reflects the relatively rapid and dynamic allocation of increased attention to emotional stimuli.

Introduction

Over four decades, researchers have utilized event-related brain potentials (ERPs) to elucidate the timing of cognitive processes (Luck, 2005, Rugg and Coles, 1996). In particular, the P300 has been used to index the relatively rapid allocation of attention following the presentation of salient stimuli. In traditional ‘oddball’ tasks, participants are asked to count or otherwise keep track of certain target stimuli; the presentation of target stimuli elicit a positivity in the stimulus-locked ERP, maximal at midline parietal sites approximately 300 ms following stimulus onset (Johnson, 1984, Johnson, 1986, Magliero et al., 1984, Squires et al., 1977, Sutton et al., 1965). Data have consistently suggested that the P300 is sensitive to directed attention toward task-relevant information (Duncan-Johnson and Donchin, 1977, Nieuwenhuis et al., 2005).

Because of their intrinsic motivational significance, emotional stimuli might be considered natural targets – automatically processed as task-relevant. In fact, early studies reported an increased P300 in the 300–500 ms post-stimulus period following the presentation of emotional compared to neutral pictures (Johnston et al., 1986, Lifshitz, 1966, Mini et al., 1996, Radilova, 1982) – an effect observed for both pleasant (Lifshitz, 1966, Mini et al., 1996, Palomba et al., 1997) and unpleasant (Lifshitz, 1966, Mini et al., 1996, Palomba et al., 1997, Radilova, 1982) pictures.

More recent work in emotion has focused on a P300-like ERP referred to as the late positive potential (LPP). The LPP is a central–parietal, midline ERP that becomes evident approximately 300 ms following stimulus onset, and is larger following the presentation of both pleasant and unpleasant compared to neutral pictures and words (Cuthbert et al., 2000, Dillon et al., 2006, Foti and Hajcak, 2008, Hajcak et al., 2006, Hajcak et al., 2007, Hajcak and Nieuwenhuis, 2006, Hajcak and Olvet, 2008, Moser et al., 2006, Schupp et al., 2000, Schupp et al., 2003, Schupp et al., 2004). Unlike the more transient P300, the LPP can be increased for several seconds following the presentation of emotional stimuli (Cuthbert et al., 2000, Foti and Hajcak, 2008, Hajcak et al., 2007, Hajcak and Nieuwenhuis, 2006, Hajcak and Olvet, 2008) and even in the period following picture offset (Hajcak and Olvet, 2008).

Principle components analyses (PCA) suggest that the sustained positivity observed following the presentation of emotional compared to neutral stimuli reflects increases in multiple midline parietal/occipital ERP positivities – including the P300 and later-peaking positivities (cf., Foti et al., in press). That is, emotional stimuli elicit an increased positivity in the time range of the P300; additionally, emotional stimuli elicit slower, later-peaking, positivities – and the combination of these components gives rise to the apparent scalp-recorded P3–LPP complex. Larger parietal positivities following emotional compared to neutral stimuli have been discussed in terms of motivated attention – the notion that emotion automatically directs attention, and thereby facilitates subsequent processing (Bradley et al., 2003, Lang et al., 1998, Morris et al., 1998, Sabatinelli et al., 2005).

Recent research has begun to examine emotion–cognition interactions, especially the interplay between directed and motivated attention, using ERPs. For example, Schupp and colleagues manipulated the task-relevance of certain types of stimuli by having participants count pleasant, neutral, or unpleasant pictures; results indicated that the difference between the P300 evoked by emotional as compared to neutral pictures was larger when emotional stimuli were also task-relevant (Schupp et al., 2007). More recently, Ferrari and colleagues presented emotional images as either targets or non-targets in a categorization task; by using the same stimuli in both conditions, Ferrari and colleagues were able to demonstrate additive effects of task relevance and emotional significance on the LPP (Ferrari et al., 2008). Keil and colleagues found similar effects, suggesting that directed attention may operate additively with emotion to evoke the LPP (Keil et al., 2005).

Moreover, studies also suggest that emotion-related increases of the P300 and LPP can be modulated by top-down regulatory processes; that is, that emotional processing can be modulated by cognitive control. For instance, Hajcak and Nieuwenhuis (2006) found that reinterpreting unpleasant images in a less negative way resulted in a reduced LPP (cf., Moser et al., 2006). More recently, Foti and Hajcak (2008) reported that the LPP elicited by unpleasant pictures was drastically attenuated when unpleasant images were preceded by more neutral than negative descriptions. Collectively, these data suggest that changing the meaning of stimuli can alter the amplitude of the LPP.

Along similar lines, Hajcak et al. (2006) found that the LPP was reduced when participants made non-affective compared to affective judgments about emotional stimuli. The authors interpreted these data as suggesting that non-affective categorization encouraged participants to attend to less emotional aspects of the images. In two related studies, Dunning and Hajcak (2009) recently found that the more sustained LPP could also be manipulated by having participants focus on more or less emotionally arousing aspects of unpleasant pictures. In both studies, the magnitude of the LPP elicited by unpleasant stimuli was reduced when participants focused on areas of unpleasant pictures that contained non-arousing content (Dunning and Hajcak, 2009).

Collectively, then, these results suggest that the P3–LPP complex may reflect the dynamic interplay between relatively automatic increases in attention to emotional stimuli and more controlled cognitive processes. The current study sought to simultaneously examine the time-course of these effects on the LPP. That is, to measure both the relatively automatic increase in the LPP elicited by unpleasant compared to neutral images, as well as the effect of online instructions to attend to more or less arousing portions of unpleasant images. To this end, participants first viewed either unpleasant or neutral IAPS images for 3000 ms; one of two tones was then presented, and served as an instruction for participants to direct their attention to either more or less arousing aspects of the images. Thus, the present design allowed for an examination of both automatic and controlled attentional processes indexed by the LPP within the same trials.

One of the attractive features of using ERPs to study neural correlates of information processing is their relatively good temporal resolution – it is possible to examine the neural changes occurring on the order of milliseconds using ERPs. Existing studies – especially on top-down attentional modulation – have scored the LPP in rather large temporal windows, and have therefore not fully capitalized on the excellent temporal resolution of ERPs. To quantify the early increase in the LPP and the subsequent modulation of the LPP by attentional instructions, we utilized the method of Guthrie and Buchwald (1991) to establish intervals in the ERP that varied as a function of picture type and instruction, respectively. In this way, then, we were able to examine whether the LPP was modulated by both automatic and controlled factors within the same trials, and could scrutinize the time-course of these effects.

Section snippets

Participants

Thirty two undergraduates (11 females, 21 males) participated in the study; none withdrew from the experiment once it begun. All the participants received course credit for their participation in the study.

Results

The grand average ERPs elicited by each picture type at the central–parietal cluster are presented in Fig. 1. Fig. 2 presents the scalp distribution of the difference between unpleasant and neutral pictures from 0 to 3000 ms, and the scalp distribution of the difference following arousing and neutral instructions on unpleasant trials from 3000 to 6000 ms. In Fig. 1, the shaded portion above the x-axis represents time-points where there was a significant paired-samples t-test (p < .05) and the solid

Discussion

In line with several previous papers, we found that the LPP was increased following the presentation of unpleasant compared to neutral IAPS (Cuthbert et al., 2000, Dillon et al., 2006, Foti and Hajcak, 2008, Hajcak et al., 2006, Hajcak et al., 2007, Hajcak and Nieuwenhuis, 2006, Hajcak and Olvet, 2008, Moser et al., 2006, Schupp et al., 2000, Schupp et al., 2003, Schupp et al., 2004). Moreover, the topography of this effect was consistent with the previous studies that have reported the scalp

Acknowledgments

The authors would like to thank Greg Siegle for sharing his MatLab scripts, and for guidance in implementing them.

References (46)

  • M.M. Bradley et al.

    Activation of the visual cortex in motivated attention

    Behav Neurosci

    (2003)
  • F. Dolcos et al.

    Event-related potentials of emotional memory: encoding pleasant, unpleasant, and neutral pictures

    Cogn Affect Behav Neurosci

    (2002)
  • C.C. Duncan-Johnson et al.

    On quantifying surprise: the variation of event-related potentials with subjective probability

    Psychophysiology

    (1977)
  • J.P. Dunning et al.

    See no evil: directing visual attention within unpleasant images modulates the electrocortical response

    Psychophysiology

    (2009)
  • V. Ferrari et al.

    Directed and motivated attention during processing of natural scenes

    J Cogn Neurosci

    (2008)
  • D. Foti et al.

    Deconstructing reappraisal: descriptions preceding arousing pictures modulate the subsequent neural response

    J Cogn Neurosci

    (2008)
  • Foti D, Hajcak G, Dien J. Differentiating neural responses to emotional pictures: Evidence from temporal-spatial PCA....
  • D. Guthrie et al.

    Significance testing of difference potentials

    Psychophysiology

    (1991)
  • G. Hajcak et al.

    Neural response to emotional pictures is unaffected by concurrent task difficulty: an event-related potential study

    Behav Neurosci

    (2007)
  • G. Hajcak et al.

    Attending to affect: appraisal strategies modulate the electrocortical response to arousing pictures

    Emotion

    (2006)
  • G. Hajcak et al.

    Reappraisal modulates the electrocortical response to negative pictures

    Cogn Affect Behav Neurosci

    (2006)
  • G. Hajcak et al.

    The persistence of attention to emotion: brain potentials during and after picture presentation

    Emotion

    (2008)
  • R. Johnson

    P300: a model of the variables controlling its amplitude

    Ann N Y Acad Sci

    (1984)
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