Elsevier

Brain Research

Volume 1239, 6 November 2008, Pages 181-190
Brain Research

Research Report
N250r and N400 ERP correlates of immediate famous face repetition are independent of perceptual load

https://doi.org/10.1016/j.brainres.2008.08.039Get rights and content

Abstract

It is a matter of considerable debate whether attention to initial stimulus presentations is required for repetition-related neural modulations to occur. Recently, it has been assumed that faces are particularly hard to ignore, and can capture attention in a reflexive manner. In line with this idea, electrophysiological evidence for long-term repetition effects of unattended famous faces has been reported. The present study investigated influences of attention to prime faces on short-term repetition effects in event-related potentials (ERPs). We manipulated attention to short (200 ms) prime presentations (S1) of task-irrelevant famous faces according to Lavie's Perceptual Load Theory. Participants attended to letter strings superimposed on face images, and identified target letters “X” vs. “N” embedded in strings of either 6 different (high load) or 6 identical (low load) letters. Letter identification was followed by probe presentations (S2), which were either repetitions of S1 faces, new famous faces, or infrequent butterflies, to which participants responded. Our ERP data revealed repetition effects in terms of an N250r at occipito-temporal regions, suggesting priming of face identification processes, and in terms of an N400 at the vertex, suggesting semantic priming. Crucially, the magnitude of these effects was unaffected by perceptual load at S1 presentation. This indicates that task-irrelevant face processing is remarkably preserved even in a demanding letter detection task, supporting recent notions of face-specific attentional resources.

Introduction

Presenting stimuli repeatedly leads to alterations in subsequent processing of the same stimuli, an effect often referred to as repetition priming. Repetition modulations cannot only be observed in behaviour (e.g., faster reaction times and improved accuracies for repeated as compared to new stimuli), but can also be established using electrophysiological or neuroimaging methods (Grill-Spector et al., 2006). One interesting and controversially discussed question is the degree to which prime stimuli can be processed, and can cause subsequent repetition modulations, even when presented in the absence of selective attention. A considerable part of this discussion has focussed on the processing of face stimuli, which may attract, or “capture”, attention to a greater extent than other stimuli (Bindemann et al., 2007b, Langton et al., 2008, Theeuwes and Van der Stigchel, 2006, but see Jackson and Raymond, 2006). Specifically, faces were sometimes found to produce repetition modulations even when not attended to at first presentation (e.g., Jenkins et al., 2002). It has also been recently suggested that faces are processed in a face-specific attentional resource (Bindemann et al., 2005, Jenkins et al., 2003).

The question of whether attention to a face might or might not be a prerequisite for implicit recognition to occur has been explored by studies using functional magnetic resonance imaging (fMRI). Stimulus repetition typically causes reduced Blood Oxygen Level Dependent (BOLD) responses to second as compared to first presentations of the image, the “repetition suppression effect”, although enhanced responses to repeated stimuli have also been reported (for a review, cf. Henson, 2003, Henson et al., 2000). With respect to the role of attention to prime faces, results were inconsistent. Henson and Mouchlianitis (2007) found repetition suppression for repeated faces (S2) only if participants attended to both first (S1) and second (S2) stimulus presentations. By contrast, Bentley et al. reported repetition decreases in occipito-temporal cortex irrespective of whether S1 faces were presented at attended or ignored positions (Bentley et al., 2003).

One reason why studies might differ in their results regarding the role of attention to prime faces on repetition effects may be the difference between studies in the experimental manipulation of attention. Specifically, the perceptual load of the tasks used in the different studies may account for the differences in the obtained results (also cf. Henson and Mouchlianitis, 2007). According to the influential Perceptual Load Theory (Lavie, 1995, Lavie, 2005, Lavie and Fox, 2000), visual perception is capacity-limited. Within this capacity, though, task-irrelevant distractor processing occurs mandatorily unless all available capacity is consumed by the task-relevant target(s). Thus, while processing of task-irrelevant distractor items is inevitable when capacity is available (i.e., low perceptual load), distractor processing should be abolished when capacity is fully recruited by target processing (i.e., high perceptual load).

Following this rationale, repetition priming by distractor faces presented in high perceptual load conditions should be abolished or at least strongly reduced. In a recent study, Jenkins et al. (2002) presented prime displays consisting of letter strings superimposed on task-irrelevant famous faces. Perceptual load in an unrelated letter search task was manipulated, and probe displays consisted of previously presented distractor faces or new famous faces. Crucially, distractor faces caused repetition priming effects (faster responses to repeated in comparison to new famous faces) of identical magnitude in both high and low perceptual load conditions. Accordingly, distractor faces were implicitly processed, irrespective of the amount of capacity recruited by the unrelated letter search task. Interestingly, however, while distractor face processing was sufficient to allow for repetition priming, it did not support explicit recognition. Rather, explicit face memory was dramatically reduced when faces had been presented as distractors under high as compared to low load conditions, consistent with the predictions from Perceptual Load Theory.

Event-related potentials (ERPs) provide a useful tool to investigate timing of cognitive processes underlying repetition effects (e.g., priming). Studies that investigated ERP repetition effects for faces frequently focussed on three ERP components as described below.

First, the N170 is a prominent response over occipito-temporal areas which is prominent for faces but is much smaller for most other visual stimuli (Bentin et al., 1996, Bentin et al., 2007, Rossion and Jacques, 2008, Thierry et al., 2007). The N170 is often thought to reflect relatively early processes in face perception related to the detection of a facial pattern, to the structural encoding of faces, or both (Eimer, 2000b, Engst et al., 2006). Evidence for the sensitivity of the N170 to face repetitions is somewhat controversial: While face repetitions did not appear to affect N170 amplitude in a majority of studies (Eimer, 2000b, Engst et al., 2006, Schweinberger et al., 2002b), other recent studies reported a small effect of repetition on N170 amplitude (Heisz et al., 2006, Itier and Taylor, 2002, Itier and Taylor, 2004, Jemel et al., 2005).

Second, the N250r is an electrophysiological correlate more consistently found for immediate face repetitions (Begleiter et al., 1995, Engst et al., 2006, Henson, 2003, Pfütze et al., 2002, Schweinberger et al., 2002b, Schweinberger et al., 2004, Schweinberger et al., 1995). This component refers to a relatively more negative ERP for repeated as compared to unrepeated faces, a difference which peaks between about 230 and 330 ms over right inferior temporal regions. This component is consistently found to be larger for familiar than unfamiliar face repetitions (Begleiter et al., 1995, Herzmann et al., 2004, Pfütze et al., 2002, Schweinberger et al., 1995) and is thought to reflect a transient activation of facial representation for face recognition (Itier and Taylor, 2004).

Third, repetitions of faces have also been shown to modulate N400-like components (Bentin and McCarthy, 1994, Cooper et al., 2007, Schweinberger et al., 2002a). The N400 is a negative ERP at centro-parietal regions, and may be the best-known ERP that is sensitive to priming. This relatively late-latency ERP is thought to be related to the semantic integration of the current stimulus into the preceding context. Consistent with this idea, N400 for faces was found to be larger for familiar as compared to unfamiliar faces (Barrett et al., 1988, Eimer, 2000a, Schweinberger et al., 1995).

So far, only few EEG studies dealt with the influence of attention to S1 faces on ERP repetition effects. In one study, Eimer (2000b) presented familiar faces, unfamiliar faces, and houses, while a 5-item alphanumeric string was centrally presented superimposed on faces and houses. In the “attended” condition, participants had to detect immediate face or house repetitions, whereas in the “unattended” condition, they had to detect a single digit in the 5-item string. In this study, N400 familiarity modulations were found for attended but not for unattended faces. Two recent studies (Martens et al., 2006, Trenner et al., 2004) compared immediate repetition effects for direct vs. indirect task conditions. In both studies, the authors found larger N250r amplitudes in a direct matching task (that is, first and second presentation were both attended and task-relevant) as compared to an indirect priming task (only second presentations were task-relevant) (Martens et al., 2006). The authors concluded that the N250r does not reflect completely automatic aspects of face processing, but is modulated by either attention or task-relevance.

All three studies compared tasks in which faces were task-relevant (and therefore supposed to be attended) with tasks in which faces were task-irrelevant (and therefore thought to be unattended). According to the Perceptual Load Theory, however, the latter assumption is not necessarily true. Even though they were task-irrelevant, faces might have been attended to in both the “indirect task” and the “detect digits” conditions, provided that attentional capacity was not fully consumed by the primary task. This has not been controlled for in either study. Moreover, the confound of task-relevance and attention makes the results difficult to interpret, such that the contribution of attention remains unclear.

To our knowledge, no study so far directly investigated effects of perceptual load manipulations to prime stimuli on repetition sensitive ERP components. Consequently, this was the main target of the current experiment. An additional benefit of manipulating attention according to Perceptual Load Theory is that it allowed us to avoid a confound of attentional effects with task-relevance. We manipulated attention in an unrelated task, while repetition priming was measured from task-irrelevant distractors only. We used an immediate repetition paradigm (Schweinberger et al., 2004) to establish the role of attention for ERP correlates of face repetitions by manipulating perceptual load to S1 faces. Participants were successively presented with pairs of images (cf. Fig. 1). S1 displays comprised of letter strings, superimposed on famous faces, and were presented for 200 ms. Participants had to identify a target letter (“X” vs. “N”) embedded either in a string of six identical letters (low load, e.g. “NNNNNN”) or in a string of six different letters (high load, e.g. “HKNWMZ”) (cf. Jenkins et al., 2005, experiment 2). Participants were explicitly instructed that S1 faces were task-irrelevant and should be ignored. S1 displays were followed by S2 displays (stimulus onset asynchrony; SOA = 2000 ms) consisting of either a repetition of the distractor face, a new famous face, or an infrequent butterfly. Participants had to respond by button press to butterflies only. Speed and accuracy was emphasised for both the letter detection task and the butterfly detection task. The butterfly detection task was included to ensure that participants attended to S2 stimuli, while enabling us to investigate face repetition effects uncontaminated by neural activity related to motor responses.

It has been shown that effects of perceptual load on attentional selection can arise during initial stages of visuocortical processing (Handy et al., 2001). If high perceptual load can prevent distractor face processing, as predicted by the Perceptual Load Theory, then we expect ERP repetition modulations to appear under low but not under high perceptual load. Behavioural evidence, though, suggested that processing of face distractors can occur to a certain extent even in high load conditions (Jenkins et al., 2002).

Assuming that this would be the case, we reasoned that an analysis of ERP repetition effects caused by task-irrelevant S1 faces presented under either low or high perceptual load would allow a relatively detailed insight into the processing of faces in the absence of selective attention. Specifically, the N170, N250r, and N400 have been related to successive stages related to structural encoding, face identification, and semantic processing, respectively. Based on previous studies of ERP face repetition effects which yielded inconclusive results, we did not have a specific prediction with respect to the N170. In the low load condition, we expected both occipito-temporal N250r effects and centro-parietal N400 effects of face repetitions similar to those described in the literature (Barrett et al., 1988, Begleiter et al., 1995, Eimer, 2000a, Engst et al., 2006, Henson, 2003, Pfütze et al., 2002, Schweinberger et al., 2002b, Schweinberger et al., 2004, Schweinberger et al., 1995). Crucially, we determined whether or not S1 faces presented under high load conditions would be able to elicit similar face repetition effects in these ERP components.

Section snippets

Behaviour

Responses were scored as correct if the appropriate response was given within 1800 ms to S1 letter strings, and within 2000 ms to S2 butterflies, respectively. To assess whether load in S1 displays was manipulated successfully, we compared response times (RTs) and accuracies to primes for high and low perceptual load conditions. Responses were faster in low load as compared to high load trials (M = 572 ms vs. M = 817 ms in low load and high load conditions, respectively; t[19] = 9.64, p < .001).

Discussion

In the current experiment, we investigated ERP correlates of repetition priming caused by task-irrelevant distractor faces presented under conditions of high or low perceptual load. According to the Perceptual Load Theory, processing of distractors should occur in low, but not in high perceptual load conditions, a pattern which has been previously demonstrated for a range of distractor stimuli including moving dot patterns (Rees et al., 1997), lexical stimuli (Lavie, 1995), or scenes (Yi et

Conclusion

We observed N250r and N400 ERP correlates of face repetitions even when task-irrelevant prime faces were presented under conditions of high perceptual load in a letter detection task. This suggests preserved access to facial identity and semantic information, respectively. Our results replicate and extend recent findings of remarkably preserved processing of faces presented outside the focus of attention (Bindemann et al., 2007a, Jenkins et al., 2002, Jenkins et al., 2003, Neumann et al., 2007

Participants

Twenty students (15 female) from the University of Jena, aged between 20 and 26 years (M = 21.8, SD = 1.9) contributed data to this study. All participants gave written informed consent and had normal or corrected-to-normal visual acuity. All participants were right-handed. One additional participant was excluded from the analyses because of technical problems in the EEG data acquisition. The study was conducted in accordance with the Declaration of Helsinki.

Stimuli and apparatus

Two hundred and eighty photographs of

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