Elsevier

Brain Research

Volume 1068, Issue 1, 12 January 2006, Pages 213-220
Brain Research

Research Report
Repetitive picture processing: Autonomic and cortical correlates

https://doi.org/10.1016/j.brainres.2005.11.009Get rights and content

Abstract

Emotionally arousing pictures elicit larger late positive potentials (LPPs) than neutral pictures during passive viewing. Moreover, these cortical responses do not rely on voluntary evaluation of the hedonic content and are relatively unaffected by task demands. In this study, we examined modulation of the late positive potential as it varies with stimulus repetition. Three pictures (pleasant, neutral, unpleasant) were presented up to 60 times each. Although the amplitude of the late positive potential during picture viewing declined with stimulus repetition, affective modulation remained intact. On the other hand, autonomic responses (skin conductance and heart rate change) habituated rapidly with stimulus repetition. These findings suggest that while stimulus detection and categorization, reflected in the LPP, is mandatory, autonomic modulation reflects initial orienting responses that habituate rapidly.

Introduction

Emotional responses are mediated by brain circuits that have evolved to organize behavior for the purpose of survival. Several studies have shown that affective pictures are effective cues in activating emotional response and suggest that affective responses serve different functions and reflect the motivational system that is engaged (i.e., defensive or appetitive) and its intensity of activation (Bradley, 2000, Lang et al., 1997). For instance, skin conductance responses are larger when viewing emotionally arousing (pleasant or unpleasant) pictures, compared to neutral pictures, covarying with the intensity parameter, whereas heart rate change varies with hedonic valence (unpleasant or pleasant), with more deceleratory heart rate responses elicited when viewing unpleasant, relative to pleasant pictures. Moreover, these responses, for the most part, habituate with repeated presentation of the same affective pictures, suggesting they index differences in initial orienting to motivationally relevant stimuli (Bradley et al., 1993).

Event-related potential studies have consistently found that emotionally arousing (pleasant and unpleasant) pictures elicit a larger late positive potential (LPP) than neutral pictures in a window from 400–800 ms after picture onset (Cacioppo et al., 1994, Cuthbert et al., 2000, Schupp et al., 2000). The magnitude of the late positive potential clearly varies with emotional arousal, with the largest LPPs elicited when viewing the most arousing emotional contents (Schupp et al., 2004). This effect has been theoretically linked to the concept of motivated attention, which proposes that motivationally significant stimuli are selectively processed because they naturally engage attentional resources (Bradley, 2000, Lang et al., 1997).

Moreover, these cortical responses do not appear to rely on voluntary evaluation of the hedonic content and are relatively unaffected by task demands. For instance, Cuthbert et al. (1995) compared the magnitude of the LPP elicited during passive viewing to when an evaluative rating task was required and found similar modulation, suggesting that passive viewing elicits similar cortical processing as an explicit evaluative task. Consistent with this reasoning, several behavioral studies have found involuntary semantic processing of affective stimuli (McKenna and Sharma, 2004, Pratto and John, 1991, Stenberg et al., 1998), as well as that affectively congruent stimuli prime both pronunciation and lexical decisions, in the absence of an explicitly evaluative context (Bargh et al., 1996, Giner-Sorolla et al., 1999, Hermans et al., 2001, Wentura, 1998).

In the current study, we examined modulation of the late positive potential as it varies with stimulus repetition, by presenting pleasant, neutral, and unpleasant pictures up to 60 times each. Past studies have found a decrement in the overall amplitude of a number of event-related potentials (ERPs) to repeatedly presented neutral stimuli (Friedman et al., 1998, Ravden and Polich, 1998). For instance, several studies (Bruin et al., 2000) have found that the N1 and P3 components decrease in amplitude as a function of stimulus repetition, with the decrease in the N1 amplitude faster than that of the P3. One theoretical interpretation of the habituation of the P3 component (Ravden and Polich, 1998) is that it reflects differences in initial orienting activity, drawing on Sokolov's theory that a mismatch between internal and external neural representations prompts orienting (Donchin and Coles, 1988, Sokolov, 1963). Habituation of P3-like potentials is more evident in passive paradigms, compared with active discrimination oddball tasks (Polich and McIsaac, 1994), and in the current study, pictures were passively viewed to optimize the possibility of observing habituation of the event-related potential.

In addition to measuring the late positive potential, we also measured skin conductance and heart rate responses, as well as reports of pleasure and arousal. We expected that the peripheral responses would habituate rapidly, evidencing differences due to the affective content of the stimuli only early in the habituation phase, as found previously (Bradley et al., 1993). Although several previous ERPs studies investigated the effect of picture content on the LPP, none have yet examined the consequence of picture repetition on the LPP. Thus, the major question is whether the late positive potential will decrease with repetition and whether, in particular, affective modulation changes with repetitive processing.

In order to attribute potential decreases in responsivity to a central, rather than to a peripheral process (e.g., fatigue), we introduced a novel set of stimuli following the habituation phase to assess reactivity and expected full recovery of all habituated responses in this phase of the experiment.

Section snippets

Self-report measures

As illustrated in Fig. 1B, arousal ratings were affected by picture repetition, picture content × block, [F(10,39) = 9.91, P < 0.001]. Reports of arousal decreased across the habituation blocks for emotional pictures (first presentation vs. block 3 [Fs(1,48) > 54, Ps < 0.001]) but remained unchanged for neutral stimuli [first presentation vs. block 3 [F(1,48) < 2, P > 0.05]. However, even after the third block, emotional pictures were rated as more arousing than neutral pictures [Fs(1,48) > 29,

General discussion

Although the amplitude of the late positive potential elicited during picture viewing was attenuated by stimulus repetition, affective modulation of the LPP remained intact. Greater cortical positivity in a window from 400–800 ms after picture onset was preserved for emotionally arousing (pleasant and unpleasant) pictures, compared to neutral stimuli, throughout a long, repetitive habituation phase. The overall decrement in the LPP across repetitions is consistent with the hypothesis that

Participants

Fifty volunteers (26 female, 22–34 years) gave written consent and participated in the study. Because the unpleasant pictures depicted a mutilated body, blood phobia was evaluated using the Mutilation Questionnaire (Klorman et al., 1974), and participants scoring above 18 were excluded. Because of computer or experimenter error, some participants were excluded from analyses of some dependent measures. Final Ns were as follows: pleasure and arousal ratings, n = 49; ERPs analysis, n = 47; heart

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