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Brain and Cognition 71 (2009) 153–164

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Directed forgetting in direct and indirect tests of memory: Seeking evidence of retrieval inhibition using electrophysiological measures Johanna C. Van Hooff a,*, T. Aisling Whitaker a, Ruth M. Ford b a b

Department of Psychology, University of Kent, Keynes College, Canterbury, Kent CT2 7NP, UK School of Psychology, Griffith University, Queensland, Australia

a r t i c l e

i n f o

Article history: Accepted 4 May 2009 Available online 24 June 2009 Keywords: Directed forgetting Event-related potentials Inhibition Selective rehearsal Recognition Lexical decision Old/new effect

a b s t r a c t We investigated whether directed forgetting as elicited by the item-cueing method results solely from differential rehearsal of to-be-remembered vs. to-be-forgotten words or, additionally, from inhibitory processes that actively impair retrieval of to-be-forgotten words. During study, participants (N = 24) were instructed to remember half of a series of presented words (TBR) and to forget the other half (TBF), as indicated by an instruction cue shown shortly after each word. During test, accuracy and reaction time measures from lexical decisions (indirect memory test) followed by recognition-memory judgements (direct memory test) were supplemented with event-related potential (ERP) recordings. Results from the behavioural measures revealed directed forgetting in the recognition-memory test but not the lexical-decision test. ERPs obtained during recognition indicated that TBR words elicited a larger parietal old/new effect than TBF words overall, suggesting that remember/forget instructions impaired conscious recollection processes more severely than familiarity processes. Moreover, TBF words that were successfully forgotten elicited less parietal activity than correctly rejected new words (the reversed old/new effect; Nowicka, A., Jednorórog, K., Wypych, M., & Marchewka, A. (2009). Reversed old/new effect for intentionally forgotten words: An ERP study of directed forgetting. International Journal of Psychophysiology, 71, 97– 102). This was taken to implicate that inhibitory processes likely affected these items. Enhanced negativities for successfully forgotten TBF words relative to new words were observed in the lexical-decision task at early (150–250 ms) and late (800–1000 ms) time windows, suggesting that inhibitory influences disrupt more than just conscious recollection when memory retrieval is tested indirectly. Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction Efficient memory functioning involves not only the successful remembering of previously presented or learned material but also the successful forgetting of irrelevant, invalid, or out-of-date information (Johnson, 1994). If undesired information is unable to be forgotten, we may find ourselves at a disadvantage. This can be the case with increasing age (Lustig, Hasher, & Tonev, 2001; Zacks, Radvansky, & Hasher, 1996) and in such clinical conditions as obsessive compulsive disorder (Wilhelm, McNally, Baer, & Florin, 1996) and post-traumatic stress disorder (Cottencin et al., 2006). The aim of the current study was to examine the brain and functional mechanisms that are involved in the forgetting of unwanted memories. More specifically, we sought behavioural and electrophysiological evidence of genuine impairment of the retrieval of such memories resulting from inhibitory processes. In the laboratory, the ability to forget is typically studied by directed forgetting procedures (for a historical review, see * Corresponding author. Fax: +44 (0) 1227 827030. E-mail address: [email protected] (J.C. Van Hooff). 0278-2626/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2009.05.001

MacLeod, 1998). These procedures provide explicit cues to indicate which presented items are to-be-remembered (TBR) and which are to-be-forgotten (TBF). These cues can be presented either after each item (item-cueing method) or after an entire list of items (list-cueing method). Regardless of which method is used, directed forgetting (DF) effects are demonstrated by poorer recall and recognition of TBF items than TBR items. For the item-cueing methods these effects are generally attributed to mechanisms operating at the encoding and storing phase, with explanations falling into two main camps. On the one hand, it has been suggested that directed forgetting stems entirely from diminished elaboration or rehearsal of TBF than TBR words. From this selective rehearsal perspective, the presentation of a remember cue encourages participants to continue their processing of the preceding word, leading to a more robust memory trace, whereas the presentation of a forget cue causes such processing to be terminated (e.g., Basden, Basden, & Gargano, 1993; Woodward, Bjork, & Jongeward, 1973). The opposing account is that an active inhibitory process is additionally brought to bear on the TBF items when the forget instruction cue is presented, suppressing their activation in working memory and inhibiting the return of attention to these items

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(e.g., Geiselman & Bagheri, 1985; Zacks & Hasher, 1994; Zacks et al., 1996). Zacks and colleagues refer to this notion as attention inhibition, whilst others refer to it as retrieval inhibition (e.g., MacLeod, 1989; Ullsperger, Mecklinger, & Müller, 2000), presumably to emphasise its detrimental effects for subsequent memory recovery. From this latter perspective, forgetting is mediated by processes that impair retrieval of TBF items over and above those processes that enhance retrieval of TBR items. 1.1. Indirect measures of directed forgetting Some researchers have evaluated the different accounts of directed forgetting by comparing outcomes for direct and indirect tests of memory. Direct memory tests, such as recall and recognition, require intentional recollection and awareness of previously presented materials. In contrast, indirect memory tests, such as word-stem completion or lexical decision, do not have these requirements and, instead, memory is inferred from a facilitation of task performance in the case of studied items (Schacter, 1987). Crucially, encoding manipulations such as level-of-processing, learning intention, or rehearsal duration, have been found to affect performance on direct memory tests but not on indirect memory tests (e.g., Graf & Mandler, 1984; Greene, 1986; Schacter & Graf, 1986). This has led to the suggestion that if directed forgetting is mediated only by differential rehearsal of TBR and TBF items then indirect memory retrieval should be similar for those two types of items and thus should show no directed forgetting effect (Basden et al., 1993; MacLeod, 1989). In opposition to this hypothesis, however, MacLeod (1989) found reliable DF effects following the itemcueing method in both direct- (recall and recognition) and indirect memory tests (word fragment completion, lexical decision), leading him to conclude that DF effects are best explained in terms of inhibitory processes. Paller (1990) and Basden et al. (1993) could not reproduce these findings though, and suggested that MacLeod’s participants may have engaged in explicit memory retrieval whilst carrying out the indirect memory tasks. Consistent with this proposal, Russo and Andrade (1995) used the process dissociation procedure (PDP) to demonstrate that remember and forget instructions affect intentional influences on memory but not automatic ones (see also, David & Brown, 2003). Whilst it seems reasonable to suppose that participants’ explicit retrieval of events from the study phase could contaminate findings from word-fragment completion tasks, such concerns may be less applicable to lexical-decision tasks given the rapidity with which word/non-word decisions are typically generated. Notably, DF effects in indirect memory tasks have since been observed by several other research groups, including those that used lexical decision as their indirect memory measure (Fleck, Berch, Shear, & Strakowski, 2001) and those that employed speeded responses and the PDP to isolate an impact of directed forgetting on automatic retrieval processes (Vonk & Horton, 2006). Many of these researchers disagreed with MacLeod’s (1989) conclusion however, and suggested that it may not be necessary to invoke notions of inhibition to explain DF effects in indirect memory tasks. For example, Fleck et al. (2001) noted that there were no negative priming effects for TBF words in their lexical-decision task (i.e., TBF words were identified more slowly than TBR words but they were still identified more quickly than new words), and thus surmised that differential excitation during retrieval might be a more likely explanation. 1.2. Electrophysiological measures of directed forgetting Another approach to seeking evidence of retrieval inhibition in directed forgetting has been to record electrophysiological brain measures such as event-related potentials (ERPs). ERPs reflect the

electrical activity of cortical brain mechanisms involved with cognitive processing (Luck, 2005). Due to their excellent temporal resolution, ERPs can provide online measures of perceptual and cognitive processing. In addition, analysis of ERP scalp distribution enables researchers to find out whether different experimental conditions engage functionally dissociable cognitive processes. In memory research, the latter strategy has often been used to investigate the differential contributions of familiarity and recollection processes in recognition judgements (e.g., Curran, 2000, 2004). Typically, recognised old items as compared to correctly classified new items elicit a more positive going ERP from 300 ms post-stimulus until approximately 800 ms. The early part of this increased positivity for old items (or decreased negativity) has a mid-frontal maximum and has been linked to familiarity processes. In contrast, the later part of the old/new effect (starting around 400 or 500 ms) has a more left-parietal maximum and is believed to reflect recollection processes (for overviews see Friedman & Johnson, 2000; Rugg, 1995). In the context of directed forgetting, recording of ERPs during recognition-memory tests should therefore make it possible to assess differences in the contribution of familiarity and recollection to participants’ responses to TBR and TBF items. More importantly, ERPs could verify whether TBF items that are successfully retrieved elicit additional activations relative to remembered TBR items, thus implicating extra processes that are needed to overcome restricted access as a result of an inhibitory mechanism (cf., Paz-Caballero & Menor, 1999; Ullsperger et al., 2000). In addition, differences in neural activations between new and TBF items that are not retrieved (i.e., successfully forgotten) might demonstrate consequences of effective inhibition of TBF items at the time of attempted retrieval (cf., Nowicka, Jednorórog, Wypych, & Marchewka, 2009). To date, only a handful of investigations have recorded ERPs during the retrieval phase in a directed forgetting paradigm using the item-cueing method (e.g., Nowicka et al., 2009; Paz-Caballero & Menor, 1999; Ullsperger et al., 2000). Although these studies produced quite different ERP results, all were taken to support the idea that an inhibitory mechanism acts upon TBF items. First, PazCaballero and Menor (1999) reported that the ERPs elicited by TBF items in a recognition-memory test were characterised by a larger early, frontal positivity (200–300 ms) and a smaller parietal old/new effect than were TBR items. Given that the early frontal effect for TBF items shortly preceded the N400, they reasoned that it might reflect ‘‘a difficulty accessing the semantic representation of these items” (p. 257), presumably as a result of an inhibitory mechanism. Furthermore, because this effect was not observed in their indirect memory task (i.e., an abstract/concrete word categorisation task for which the DF effect was similarly absent), they speculated that such an inhibitory mechanism might operate only when conscious access to the previous learning episode is required (cf., Bjork & Bjork, 1996). Second, Ullsperger et al. (2000) found topographical ERP differences between TBR and TBF items at time of retrieval which were not observed between deeply- vs. shallowly-encoded items, despite similar behavioural outcomes. In particular, TBF items did not elicit the typical parietal old/new effect but instead elicited a late right-frontal old/new effect after the responses had been made. Ullsperger and colleagues suggested that this late, right-frontal effect might reflect post-retrieval mechanisms that were recruited to access previously inhibited items that could not readily be retrieved (i.e., supporting release from inhibition). They concluded that the absence of a similar ERP modulation for deeply- and shallowly-encoded words meant that selective rehearsal alone could not account for the observed DF effects in their behavioural measures. Finally, Nowicka et al. (2009) investigated the processes that lead to successful forgetting by examining ERPs for TBF items that either were or were not retrieved in the test phase. They found that

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TBR-remembered trials elicited a typical old/new effect (500– 750 ms post-stimulus) over central and parietal areas that was lacking for TBF-remembered items. Additionally, TBF-forgotten items were shown to elicit ERPs that were more negative going in the 500–750 ms time window than were ERPs for correct rejections, a phenomenon they termed ‘the reversed old/new effect’. Nowicka et al. concluded that TBR-remembered items were more likely than TBF-remembered items to give rise to a sense of conscious recollection during memory retrieval. They further speculated that the reversed old/new effect for TBF-forgotten items might reflect processes associated with intentional and effective inhibition. 1.3. The present study The present study sought to clarify the underlying mechanisms of DF effects in the item-cueing paradigm by using a combination of the behavioural and electrophysiological methods described above. Participants undertook a standard item-method DF procedure and subsequently completed first a lexical-decision test and then a recognition-memory test that evaluated the accuracy and latency of their responses to TBR vs. TBF words. Lexical decision was selected as our indirect memory measure on the grounds that (1) this technique minimises the likelihood of explicit retrieval strategies (Basden et al., 1993; Fleck et al., 2001), and (2) lexical decision and recognition-memory tasks use similar presentation formats and can be used to generate similar outcome measures (namely RT and ERP). ERPs were recorded during both the indirect and direct memory tasks, making it possible to investigate the impact of DF instructions on priming in the former case and familiarity vs. recollection processes in the latter. In addition, in an extension to the work by Nowicka and colleagues (2009), ERPs and behavioural responses were compared between TBF items that were successfully retrieved vs. those that were not retrieved both for the recognition test itself and for the preceding lexical-decision task. On a behavioural level, we expected to demonstrate a DF effect in the recognition-memory test regardless of whether we found evidence of an inhibitory mechanism in the physiological data given participants’ enhanced rehearsal of TBR items relative to TBF items. For the lexical-decision test we sought to determine whether conclusions about the impact of DF instructions on priming were affected by subsequent recognition status of TBR vs. TBF words (i.e., remembered vs. forgotten). On a physiological level, we predicted that a contribution of inhibitory mechanisms to item-method directed forgetting in recognition memory should be revealed in either (1) unique ERP activations for TBF- relative to TBR words that are successfully retrieved, for example, an increased early, frontal positivity for remembered TBF words (cf., Paz-Caballero & Menor, 1999) or an increased late, right-frontal positivity for remembered TBF words (cf., Ullsperger et al., 2000), or (2) a reversed old/new effect for TBF words that are successfully forgotten (cf., Nowicka et al., 2009). Similar analyses were conducted on the ERP data for the lexical-decision task to see whether inhibitory influences that might be active for TBF items are limited to memory tests that make explicit reference to the previous learning period (cf., Bjork & Bjork, 1996; Paz-Caballero & Menor, 1999).

2. Method 2.1. Participants Twenty-five native English speakers were recruited from the University student population. They were paid £5 per hour for their participation. Data from one participant could not be used due to

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difficulty with the task presentation software. The remaining 24 participants comprised 12 males and 12 females, ranging in age from 18 to 35 years (Mean 22.2 years, SD 3.8). All participants were right handed, as determined by the Edinburgh Handedness Inventory (Oldfield, 1971). Treatment of participants was in accordance with APA and BPS ethical guidelines and approval for the study was granted from the local Research Ethics Committee. All participants gave their informed consent before the start of the experiment. 2.2. Stimulus materials Stimuli consisted of 360 one-syllable nouns, selected from the online MRC psycholinguistic database (http://www.psy.uwa.edu.au/mrcdatabase/uwa_mrc.htm). The words were 3–6 letters in length and were characterised by a low written occurrence frequency (1–40, Kucera & Francis norms) and high concreteness (500–700) (norms as implemented in the online MRC psycholinguistic database). Highly typical exemplars of particular semantic categories were excluded to avoid facilitation and interference effects. This was achieved by selecting words that had response proportions smaller than 0.40 on the Van Overschelde, Rawson, and Dunlosky (2004) category norms. Stimuli were presented in lowercase (28-point Arial font) and were centrally displayed in white on a black background. Words were divided into six separate lists of 60 words each (lists i–vi), which were matched in terms of frequency, concreteness, and word length. The usage of these lists for the three experimental tasks was rotated between participants. Additionally, 240 one-syllable non-words with 3–6 letters were used in the lexical-decision task. The non-words were taken from both the ARC non-word database (Rastle, Harrington, & Coltheart, 2002) and from a list compiled by Ferraro and Kellas (1990). EPrime software was used to present the stimuli and to record the behavioural data. 2.3. Experimental tasks The experiment consisted of three tasks that were carried out in the same order for all participants, namely, (1) study task, (2) lexical-decision task, and (3) recognition-memory task. An orienting prompt (*****) was presented at the beginning of each task in the centre of the screen for 1000 ms, followed by a blank screen for 500 ms. 2.3.1. Study task Two lists of 60 words each were presented in the study task. Words from one of these lists were followed by a remember instruction (RRRR) and words from the other list were followed by a forget instruction (FFFF). The words were presented in a pseudorandom sequence with the restriction that four or more words from the same list (and thus followed by the same instruction) never occurred consecutively. Each word was presented for 500 ms, followed by a blank screen (2000 ms) and then the instruction cue (500 ms). The time between offset of the instruction cue and onset of the subsequent stimulus word was 2000 ms. Two buffer words followed by a remember instruction were presented at the beginning and at the end of the study task, which were excluded from subsequent analyses. 2.3.2. Lexical-decision task The lexical-decision task consisted of presentation of the 120 study words (e.g., list i and ii), randomly intermixed with 120 new words (e.g., list iii and iv) and 240 non-words. Half the study words were TBR words and the remainder were TBF words. Participants were requested to judge each stimulus as being either a word or a non-word by pressing the appropriate button on the serial response box using the index fingers of their left and right

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hands (button assignments were counterbalanced between participants), with no mention being made of the fact that some of the words had been presented during the study task. They were instructed to respond as quickly and as accurately as possible. Stimuli remained on the screen until a response had been made. The subsequent stimulus appeared 1000 ms after participants made their response. 2.3.3. Recognition-memory task The recognition-memory task involved presentation of the 120 study words (e.g., list i and ii) randomly intermixed with another set of 120 new words (e.g., list v and vi). Participants were requested to judge each stimulus as being either old or new by pressing the appropriate response button using the index fingers of their left and right hands (old/new buttons corresponded to word/nonword buttons in the previous task). Again, they were instructed to respond as quickly and as accurately as possible. It was made clear to participants that they were being asked to distinguish between: (1) words that had appeared in the study list regardless of whether they had been followed by a remember or forget instruction and (2) words that had never appeared in the study list. Again, stimuli remained on the screen until a response was made, with the subsequent word appearing 1000 ms later. 2.4. Procedure Participants were tested individually and were asked to relax as much as possible and to make no excessive movements. For the study task, they were requested to memorise the words followed by a remember instruction (TBR words) and to forget the words followed by a forget instruction (TBF words). Participants were falsely led to believe that only their memory for the TBR words would be tested and that, because the list was so long, it would be beneficial to forget the other words. To reinforce these instructions, a monetary reward (£20) was offered at this stage for the person who achieved the highest score for TBR words on the subsequent memory test. Following the study task, participants were verbally instructed to complete a filler task of counting backwards aloud in multiples of 3 from 100. They were then asked to perform the lexical-decision task in the guise of an additional filler task. After completion of the lexical-decision task, participants were offered a break of approximately 5 min to relax before undertaking the recognition-memory test. 2.5. Electrophysiological recording and analysis EEG data were continuously recorded (average reference) from 19 Ag–AgCl electrodes mounted in an elastic cap (Easy Cap QA40): Fp1, Fp2, F7, F3, Fz, F4, F8, C3, Cz, C4, T3, T5, T4, T6, P3, Pz, P4, O1, O2. Two ear-clip electrodes were used to record activity from the earlobes (A1, A2). Two bipolar Ag–AgCl electrodes were placed above and below the participant’s left eye to record vertical eye movements and blinks. All electrode locations were first cleaned with isopropyl-alcohol (70%) before an abrasive electrolyte gel (Abralyt) was used to gently remove any dead skin cells and to conduct the electrical activity. Inter-electrode impedance was kept below 8 kOhm. EEG and EOG signals were amplified using a Quickamp 72 amplifier and Brain Vision Recording software (version 1.02). The data were recorded with a sample rate of 250 Hz and a bandpass filter of 0.1 and 35 Hz (24 dB). EEG data were corrected off-line for eye movements using the Gratton and Coles (1989) method, as implemented in the BrainVision analysis software. Recordings were then re-referenced to a mathematically simulated linked ears reference (A1, A2). EEG recordings were automatically screened for artefacts using the following criteria: (a) maximum allowed voltage step of 50 lV between two sample points, (b) max-

imum allowed absolute difference of 80 lV over a 200 ms interval, and (c) lowest allowed activity of 0.5 lV over a 100 ms interval. EEG data containing artefacts in any of the recording channels were rejected from further analyses. EEG epochs were created from 100 ms prior to stimulus onset to 1500 ms following stimulus onset. These epochs were baseline corrected to a pre-stimulus baseline of 100 ms. For the lexical-decision task, EEG epochs (correct lexical decision responses only) were averaged according to stimulus category (TBR, TBF, New) and for the TBF items, also according to whether they were subsequently recognised or not (TBF-r, TBF-f). For the recognition-memory task, a similar calculation of ERPs was performed, resulting in distinct ERPs for: (a) recognised TBR items (TBR-r), (b) recognised TBF items (TBF-r), (c) not-recognised or forgotten TBF items (TBF-f), and (d) correctly rejected New items (CR-new). ERPs were considered reliable when they were composed out of more than 16 individual EEG trials. As a consequence, ERPs for TBR-f items could not be calculated for most participants (due to a high level of recognition performance) and were therefore not included in the analyses. Mean ERP amplitudes were quantified and statistically tested for three frontal (F3, Fz, F4), three central (C3, Cz, C4), and three parietal (P3, Pz, P4) electrode positions. These electrode positions allowed us to examine scalp distribution effects in anterior–posterior and medial–lateral directions. The ERP old/new effect was quantified as the mean amplitude of three 200 ms time windows. The first time window (300–500 ms) was considered to encompass the early, frontal old/new effect associated with familiarity processes. The second time window (500–700 ms) was considered to include the late, parietal old/new effect associated with recollection (Rugg & Curran, 2007). A final 200 ms time window (800– 1000 ms) was included to cover post-retrieval evaluation and monitoring processes (Allan, Wilding, & Rugg, 1998; Hayama, Johnson, & Rugg, 2008). The ERP mean amplitudes were analysed with repeated-measures ANOVAs that included stimulus type (TBR/TBF/ New or TBR-r/TBF-r/CR-new or TBF-r/TBF-f/CR-new), anterior–posterior position (frontal, central, parietal), and Laterality (left, midline, right) as within-subjects factors. All effects with more than one degree of freedom were adjusted for sphericity violations using the Greenhouse Geisser method. Because of easier notification, however, uncorrected degrees of freedom are reported. If applicable, main effects were followed up by pairwise comparisons with Bonferroni correction. To avoid describing large amounts of statistical data concerning scalp distribution effects, only main effects or interactions with the factor stimulus type are reported.

3. Results 3.1. Behavioural data Table 1 presents means and standard deviations of verification accuracy and response latency (RTs) for the lexical-decision test, shown separately for TBR-r, TBF-r, TBR-f, TBF-f, and New words. RTs for New words refer to those words that were correctly endorsed in the lexical-decision test (CE-new). Table 2 presents means and standard deviations of response latency (RTs) for the recognition-memory test, again shown separately for TBR-r, TBFr, TBR-f, TBF-f, and New words. RTs for New words refer to those words that were correctly rejected in the recognition-memory test (CR-new). 3.1.1. Lexical-decision task Repeated-measures ANOVAs on the verification accuracy data revealed a significant effect of stimulus type when comparing new words with remembered old words (New vs. TBR-r vs. TBF-

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Table 1 Means and standard deviations (in parentheses) of proportional accuracy and RTs for the lexical-decision task as a function of stimulus type and subsequent recognition performance. New

Verification accuracy RT (ms)

Remembered old items

0.92 (0.07) 657 (117)

Forgotten old items

TBR-r

TBF-r

TBR-f

TBF-f

0.96 (0.03) 637 (110)

0.96 (0.05) 624 (112)

0.93 (0.11) 683 (172)

0.92 (0.08) 660 (132)

Note: RTs were calculated for items that were correctly identified as words.

Table 2 Means and standard deviations (in parentheses) of RTs for the recognition-memory task as a function of stimulus type and accuracy.

3.2. Electrophysiological data

the three types of items (this was also the case for other electrode positions not shown in this Figure), an observation confirmed by non-significant main- and interaction effects of stimulus type (TBR vs. TBF vs. New) on the pre-defined amplitude measures (300–500 ms, 500–700 ms, 800–1000 ms). Similar null findings emerged when comparing TBR-r words, TBF-r words, and New words (Fig. 1b; N = 19). The mean numbers of EEG trials that contributed to these ERPs were 38.3 for TBR-r words, 27.8 for TBF-r words, and 100.9 for New words. The absence of a parietal old/ new effect suggests that old items were not incidentally recollected in the indirect test (cf., Curran, 1999; Paller, Kutas, & McIsaac, 1995). To see whether ERPs differed as a function of subsequent recognition-memory performance, results were compared for New words and TBF words which were remembered (TBF-r) and which were forgotten (TBF-f), respectively, (see Fig. 1c) (too few participants generated a high proportion of forgotten TBR trials to enable a comparison of ERPs between TBR-r and TBR-f words). These grand averages and subsequent analyses were based on 13 participants for whom enough EEG trials could be collected for both types of TBF words (>16 artifact-free EEG epochs). The mean numbers of EEG trials that contributed to these ERPs were 27.7 for TBF-r items, 23.1 for TBF-f items, and 103.8 for New items. As indicated in Fig. 1c, compared to TBF-r and New items, TBF-f items elicited more negative amplitudes in an early time window overlapping the N2 component (150–250 ms), a middle time window encompassing the old/new effect (400–600 ms), and a late time window possibly related to decisional or monitoring processes (800– 1000 ms). To test these observations, mean amplitudes were calculated for these intervals in addition to those that were predefined based on previous literature (i.e., 300–500 ms, 500–700 ms). Repeated measures ANOVAs were performed on these mean amplitudes with stimulus type (TBF-r, TBF-f, New), anterior–posterior position (frontal, central, parietal), and laterality (left, midline, right) as within-subjects factors. Marginally significant effects of stimulus type were found for the mean amplitudes in the 150–250 ms (F(2, 24) = 3.60, p = 0.06) and 800–1000 ms (F(2, 24) = 2.81, p = 0.09) time windows. For these same amplitude measures, significant stimulus type  laterality interactions were found (150–250 ms: F(4, 48) = 3.45, p < 0.05; 800–1000 ms: F(4, 48) = 2.97, p < 0.05), revealing that effects of stimulus type were generally largest for left- and midline-electrode positions. In all cases, the effects of stimulus type were driven by more negative amplitudes for TBF-f items as compared to New items and TBF-r items (see Fig. 2). Although apparent in Fig. 1c, stimulus type did not significantly affect the mean amplitudes in the 400–600 ms interval (F(2, 24) = 1.85, p = 0.19), nor in any of the other intervals (300–500 ms, 500–700 ms).

3.2.1. Lexical-decision task Grand average ERPs from three midline-electrode positions for the lexical-decision task are shown in Fig. 1a (N = 24). The mean numbers of EEG trials that contributed to these ERP waveforms were 55.5 for TBR words, 54.3 for TBF words, and 106 for New words. As can be seen, ERP waveforms were highly similar across

3.2.2. Recognition-memory task Fig. 3 shows the grand average ERP waveforms at three frontal, three central, and three parietal electrode positions (left, midline, right) elicited by TBR-r, TBF-r, and CR-new words in the recognition-memory task (N = 21). Data from three participants had to be excluded due to an insufficient number of EEG trials for the

New

RT (ms)

942 (279)

Remembered old items

Forgotten old items

TBR-r

TBF-r

TBR-f

TBF-f

834 (217)

904 (305)

1042 (428)

1029 (396)

r; F(2, 46) = 7.55, p < 0.01) but not when comparing new words with forgotten old words (New vs. TBR-f vs. TBF-f; F(2, 46) = 0.415, p = 0.59). Pairwise comparisons in the former case showed that New items were verified less accurately than either TBR-r items (p < 0.05) or TBF-r items (p < 0.01), whereas verification accuracy did not differ significantly between TBR-r and TBFr items (p = 1.00). Similar results were obtained in relation to the RT data, showing a significant effect of stimulus type only when comparing CE-new words with old words that were remembered in the subsequent recognition-memory test (F(2, 46) = 7.88, p < 0.01). Pairwise comparisons revealed that both TBR-r (p = 0.09) and TBF-r items (p < 0.01) were responded to more rapidly than CE-new items, whereas there were no significant differences in response latency between TBR-r and TBF-r items (p = 0.40). These results indicate that priming was restricted to remembered old words and, moreover, that the DF effect failed to emerge in the lexical-decision test regardless of whether TBR and TBF words were subsequently endorsed in the recognitionmemory test. 3.1.2. Recognition-memory task A paired samples t-test revealed that, as expected, the proportion of remember responses for TBR items (Mean 0.76, SD 0.11) was higher than for TBF items (Mean 0.58, SD 0.16) (t(23) = 6.49, p < 0.001). Additionally, RTs for remembered TBR words were significantly faster than for remembered TBF words (t(23) = 2.61, p < 0.05). Thus, the DF effect was detectable for both recognitionmemory accuracy and recognition-memory speed. Effects of the DF instruction were further investigated by comparing RTs for CR-new items, TBR-f items, and TBF-f items. A significant effect of stimulus type (F(2, 46) = 3.25, p < 0.05) revealed that rejection latencies to CR-new items were marginally faster than to either TBR-f items (p = 0.16) or TBF-f items (p = 0.08), whereas rejection latencies to the latter two types of item did not differ significantly (p = 1.00). These results indicate that the DF effect did not manifest itself as speedier rejections of actively than passively forgotten words.

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Lexical decision task Fz

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TBF-r stimulus category. The mean numbers of trials that contributed to these waveforms were 44.5 for TBR-r, 35.4 for TBF-r, and 93.3 for CR-new words, respectively. A clear old/new effect could be observed for the remembered TBR words (TBR-r) whilst a smaller one seemed to be present for the remembered TBF words (TBFr). In accord with the literature (e.g., Rugg, 1995; Rugg & Curran, 2007) this old/new effect encompassed an early negative wave (300–500 ms) followed by a left-lateralised, centro-parietal positive wave (500–700 ms). Unlike the ERP results reported by PazCaballero and Menor (1999), TBF-r items in this experiment did not elicit an additional early frontal positivity. Furthermore, in contrast to Ullsperger et al. (2000), only a very small late frontal old/ new effect (800–1000 ms) could be observed, which differed little in magnitude between TBR-r and TBF-r items. Mean amplitude values for the three distinct 200 ms time windows are depicted in Fig. 4. These mean amplitudes are averaged over the nine electrode positions that were used in the statistical analysis (F3, Fz, F4, C3, Cz, C4, P3, Pz, P4). Stimulus type (TBR-r vs. TBF-r vs. CR-new) was found to significantly affect mean amplitudes in both the 300–500 ms (F(2, 40) = 7.20, p < 0.01) and the 500–700 ms (F(2, 40) = 4.10, p < 0.05) time window. For the first time window (300–500 ms), pairwise comparisons showed that both TBR-r (p < 0.01) and TBF-r (p < 0.05) words elicited less negative waveforms than CR-new words. For the second time window (500–700 ms), only the mean amplitudes for TBR-r words were reliably more positive than those for CR-new words (p < 0.01). Significant early old/new effects (300–500 ms) were thus present for both types of remembered old items (TBR-r and TBF-r), whilst

the late old/new effect (500–700 ms) was present for TBR-r items only. For both these time windows a significant interaction between stimulus type and laterality was found (300–500 ms: F(4, 80) = 3.66, p < 0.05; 500–700 ms: F(4, 80) = 3.36, p < 0.05) revealing that, in general, the observed old/new effects were less pronounced over the right hemisphere electrode positions as compared to their midline and left counterparts. The last time window (800–1000 ms) showed no main effect of stimulus type but, instead, a significant stimulus type  anterior–posterior position interaction (F(4, 80) = 5.37, p < 0.05). Mean amplitude values revealed that the effect of stimulus type (TBR-r vs. TBF-r vs. CRnew) was larger over the frontal- than central- and parietal-electrode positions. The main effect of stimulus type, however, remained non-significant when only the frontal electrode positions were included in the analyses (F(2, 40) = 2.26, p = 0.13). To investigate the processes involved in successful forgetting, a second series of analyses was performed comparing ERPs for CRnew items with those for TBF items which were remembered (TBF-r) and which were forgotten (TBF-f), respectively, (N = 15). Corresponding grand average ERP waveforms are depicted in Fig. 5. The mean numbers of trials contributing to these waveforms were 33.5 for TBF-r, 24.5 for TBF-f, and 93.4 for CR-new items. The ERP old/new effect for TBF-r items, as discussed previously, could still be observed. Notably, TBF items that were successfully forgotten seemed to elicit even less positive amplitudes than the CR-new items, particularly during the 500–700 ms time window. For the 300–500 ms time window, the effect of stimulus type (TBF-r vs. TBF-f vs. CR-new) was marginally significant

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In agreement with earlier studies, TBR words were recognised more frequently than TBF words (Basden et al., 1993; Lee, Lee, & Tsai, 2007; Zacks et al., 1996) and also more quickly (Fleck et al., 2001; Nowicka et al., 2009). This demonstrates that participants correctly followed instructions and that our directed forgetting manipulation was effective, despite the fact that all studied words were re-exposed during the preceding lexical-decision test. Moreover, the concordance between the accuracy and latency measures indicate that the impact of the remember/forget instructions on recognition performance cannot be dismissed as a change in speed/accuracy trade-off. In contrast, there was no evidence of superior verification accuracy or faster response latencies for TBR relative to TBF items during lexical decisions, regardless of whether the DF effect was evaluated for words that were subsequently endorsed in the recognition-memory test or for words that were subsequently rejected (i.e., no DF effect in either case). The findings from our indirect task failed to replicate those reported by MacLeod (1989) and Fleck et al. (2001) who used a similar lexical-decision procedure and comparable remember/forget instructions. It is worth noting though, that RT facilitations for TBF words overall were highly comparable across investigations, varying in absolute terms from 17 ms in the study by Fleck et al. (2001), to 19 ms in the current study, and 20 ms in the study by MacLeod (1989). Thus, inconsistent DF effects appear to reflect differences in the extent of enhancement of TBR items rather than of impairment of TBF items.

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(F(2, 28) = 2.76, p = 0.09), revealing that, on average, mean amplitudes in this time window were less negative for TBF-r items than for TBF-f and CR-new items. For the 500–700 ms time window, a significant main effect of stimulus type was found (F(2, 28) = 3.94, p < 0.05) as well as a significant stimulus type  anterior– posterior position interaction (F(4, 56) = 4.73, p < 0.05). Overall, amplitudes for TBF-f words were less negative than those for TBF-r and CR-new words, although none of these pairwise comparisons reached significance. Follow-up ANOVAs for the frontal, central-, and parietal-electrode positions separately showed that the effect of stimulus type was significant for the central (F(2, 28) = 4.87, p < 0.05) and parietal- (F(2, 28) = 8.73, p < 0.01) electrode positions but not for the frontal ones. Pairwise comparisons for the central electrodes revealed that TBF-f words elicited less positive amplitudes than did the TBF-r (p = 0.06) and CR-new (p < 0.05) words. Similarly, for the parietal-electrode positions, mean ERP amplitudes for TBF-f words were less positive than those for TBF-r (p < 0.01) and CR-new (p = 0.06) words. The mean amplitudes for the three stimulus categories are displayed in Fig. 6 as a function of anterior–posterior electrode position (averaged over left-, midline-, and right-electrode positions).

Despite behavioural priming effects for both TBR-r and TBF-r items in the lexical-decision test, no similar priming could be demonstrated at ERP level. Some ERP studies have reported that repeated items, in conditions that did not require explicit retrieval, evoked a small increased positivity with a centro-parietal maximum within the 300–500 ms time window (e.g., Boehm, Sommer, & Lueshow, 2005; Paller & Gross, 1998). This ERP modulation was found to be unaffected by the level of processing during encoding and has also been observed for unrecognised items (Rugg et al., 1998). Other studies, however, have failed to show such an ERP priming effect during either a word/non-word discrimination task (Walla, Endl, Lindinger, Deecke, & Lang, 1999) or a word-stem completion task (Kane, Picton, Moscovitch, & Winocur, 2000). Thus, an ERP correlate of implicit memory has not consistently been observed in previous studies, suggesting that it may be difficult to obtain when, like in our study, behavioural priming effects are small. We nevertheless conclude that behavioural priming of the studied items in the current study was genuinely driven by implicit memory, given other aspects of the ERP data to suggest that participants rarely became aware of the re-presentation of studied material during the lexical-decision task. Specifically, the absence of a parietal old/new effect for either TBR or TBF words, regardless of their subsequent recognition status, suggests that the studied items were not incidentally recollected. According to Curran (1999), the late parietal old/new effect (labelled P600 in his study) can occur independently of retrieval intention, suggesting that the recollection processes reflected in this component relate at least partly to ‘‘recollected information [that] may come to mind incidentally or involuntarily” (Curran, 1999, p. 781; see also Paller et al., 1995). As discussed in the introduction, previous behavioural studies have produced inconsistent results with regards to DF effects on indirect memory tests and it has been argued that contamination by explicit retrieval may be responsible for DF effects in indirect tests when such effects do occur (Basden et al., 1993;

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David & Brown, 2003; Paller, 1990; Russo & Andrade, 1995). Our findings are in agreement with this conclusion, failing to produce

behavioural evidence of directed forgetting in a lexical-decision task for which accompanying ERPs produced no evidence that participants experienced conscious recollection of the studied items. On the other hand, ERPs for the lexical-decision task revealed an impact of DF instructions on cognitive processes not dedicated to retrieval of episodic memories, at least when evaluating findings for TBF words that were subsequently rejected in the recognition-memory test. Specifically, we observed more negative ERP amplitudes for TBF-f words than for either TBF-r words or new words in early (150– 250 ms) and late (800–1000 ms) time windows, particularly over left and midline areas. The timing of the early effect suggests that it may index differential activations of the lexical pathway. Previous ERP studies of single-word reading and lexical-decisions have documented a negative lexicality effect peaking around 170 ms and, importantly, have demonstrated that such an effect is accentuated with the difficulty of lexical access (for review see Dien, 2009). For example, greater negativities have been reported for low-frequency than for high-frequency words (Sereno, Rayner, & Posner, 1998) and for derived than for non-derived pseudowords (Proverbio & Adorni, 2008). Because ERPs for TBF-r words were similar to those elicited by new words in the present study, such findings suggest that enhanced negativity to TBF-f words can be attributed to processes that impeded their lexical access, such as inhibitory processes. Consistent with this conclusion, studies of selective attention have linked increased N2 amplitudes to heightened attention to relevant stimulus features (e.g., Anllo-Vento, Luck, & Hillyard, 1998).

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In contrast, the more negative amplitudes to TBF-f at 800– 1000 ms might reflect diminished activity of post-decision processes pertaining to such items. Moreover, in the context of recognition-memory studies, correctly endorsed old items are often observed to display more positive-going ERPs than do correctly rejected new items in the late time window, albeit more commonly right- than left-lateralized. Hayama et al. (2008) recently reported that this effect does not necessarily depend on retrieval of information from episodic memory and concluded that it may reflect one of two things: (1) generic monitoring or decisional processes, or (2) evaluation of memory retrieval for either episodic or semantic information. Applied to the present findings, both suggestions are consistent with the notion that TBF-f words might have been relatively difficult to process during the indirect test as a consequence of inhibition, resulting in an attenuated late positivity. Further study is needed to corroborate this suggestion though, particularly given the fact that it was recorded during an indirect and not direct memory task and also because of its distinct scalp distribution. Regardless of the outcomes of such studies, however, both the early and late effects for TBF-f words suggest that forget instructions might impair more than just conscious memory retrieval.

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4.2. Directed forgetting in recognition memory: electrophysiological evidence Consistent with the behavioural outcomes, ERP data associated with correct recognition-memory decisions indicated a larger old/ new effect for TBR-r than TBF-r words. This finding accords with previous ERP studies of directed forgetting reporting diminished or even absent old/new effects for TBF words (Nowicka et al., 2009; Paz-Caballero & Menor, 1999; Ullsperger et al., 2000). In our study, the reduced old/new effect for TBF-r words was most evident for the 500–700 ms time window, suggesting that recognition responses for TBF-r items were based more on familiarity than recollection. The proposal that forget instructions diminished the likelihood that participants experienced conscious recollection of TBF words would be consistent with findings reported by Gardiner, Gawlik, and Richardson-Klavehn (1994), which revealed that learn-vs.-forget instructions influenced ‘remember’ but not ‘know’ responses (see also Basden & Basden, 1996, Experiment 3). Importantly, differential effects on recollection and familiarity have also been reported in depth-of-processing studies (Yonelinas, 2002). For example, Rugg and colleagues (1998) reported that the early old/new effect was of equivalent magnitude for recognised items that received deep processing during study (sentence generation) rather than shallow processing (alphabetic judgement), whereas the parietal old/new effect was present only for items that were deeply processed. Likewise, Curran (2004) observed that the frontal old/new effect (FN400) was not reduced by divided attention, whereas the parietal old/new effect was. Such findings suggest that the augmented parietal old/new effect for TBR-r words was driven largely by their more extensive rehearsal during the study phase, although inhibitory influences acting upon TBF items cannot be excluded on the basis of these results. Whilst differential rehearsal was undoubtedly an important factor in superior recognition of TBR than TBF words, ERPs for TBF items that were successfully forgotten were suggestive of an additional, inhibitory mechanism contributing to directed forgetting. In agreement with Nowicka et al. (2009), we found that TBF-f words evoked less positive amplitudes in the 500–700 ms time window than either TBF-r words or correctly rejected new words, thus showing a reversed old/new effect. Nowicka and colleagues interpreted the reversed old/new effect in their study as reflecting intentional and effective inhibition of TBF-f items. A specific mechanism that could account for these results is that remember/forget instructions at encoding determine how much attention will be assigned to TBF and TBR items during explicit memory retrieval. Moreover, Dywan and colleagues suggested that the posterior old/new effect might index attention allocation rather than remembering per se (Dywan, 2000; Dywan, Segalowitz, & Arsenault, 2002; Dywan, Segalowitz, & Webster, 1998; Herron & Rugg, 2003) and hence the reversed old/new effect for TBF-f items suggests that the forget instruction successfully inhibited the return of attention to these items (cf., Geiselman & Bagheri, 1985; Zacks & Hasher, 1994; Zacks et al., 1996). An alternative account of the reversed old/new effect should be considered, however. Namely, it is known that the generators of the P3 component contribute to the parietal old/new effect (Spencer, Vila Abad, & Donchin, 2000) and that the P3 is sensitive to response confidence (Polich & Kok, 1995). The relatively small late positivity for forgotten TBF items (giving rise to the reversed old/ new effect) might thus have been the result of the low confidence levels with which these classifications were made. Indeed, such interpretation is supported by our RT results, showing the longest response latencies for the not-recognised old items (see Table 2). Curran (2004), however, demonstrated that higher confidence levels increased the late parietal positivities for old items but not those for new items. He therefore concluded that the parietal

old/new effect is not well explained ‘‘by confidence differences arising from generic decision processes” and that it more likely reflects a high-threshold recollection process (Curran, 2004, p. 1102; for a contrasting view, see Finnigan, Humphreys, Dennis, & Geffen, 2002). Thus, the reversed old/new effect for TBF-f items cannot fully be explained by reduced decision confidence without any reference to impaired recollection, either as a result of reduced rehearsal or inhibitory influences. In the recognition task, ERP activations before and after the old/ new effect for recognised old items (TBR-r and TBF-r) did not reveal any compelling evidence of the presence of an inhibitory mechanism acting upon the TBF-r items, as was previously observed by Paz-Caballero and Menor (1999) and Ullsperger et al. (2000). Specifically, we failed to reproduce their key findings for TBF-r items, that is, (1) the presence of an early frontal positivity (200–300 ms), believed to reflect more difficult access to semantic representations (Paz-Caballero & Menor, 1999) and (2) the presence of a post-retrieval right-frontal positivity (950–1200 ms) believed to reflect additional mechanisms activated to overcome inhibition (Ullsperger et al., 2000). One obvious explanation of why we did not find these early and late effects is the repeatedmeasures nature of our study, raising the possibility that impaired access to TBF items was ameliorated by their re-exposure in the lexical-decision task. However, the failure to replicate the post-retrieval right-frontal positivity observed by Ullsperger et al. (2000) might also reflect differences in the methods used to induce directed forgetting. Unlike most studies of directed forgetting employing the itemcued paradigm, Ullsperger and colleagues presented study blocks of 30 words each rather than a single, lengthy study list. These study blocks were separated from each other by 60 s during which participants were asked to write down as many TBR words as possible. This was done to ‘‘strengthen the differential instruction for TBR and TBF items” (p. 936) but it could be argued that this additional requirement enhanced the operation of the inhibitory mechanism via a process of retrieval-induced forgetting (RIF).1 RIF refers to the phenomenon that retrieval of a subset of previously studied material can cause subsequent forgetting of the non-retrieved material (e.g., Anderson, Bjork, & Bjork, 1994; Bäuml, Zellner, & Vilimek, 2005; Hicks & Starns, 2004). It is widely assumed that this type of forgetting is caused by retrieval inhibition, such that retrieving a subset of studied material invokes an inhibitory process that counteracts interference from the remaining studied items (for a review see Anderson, 2003). Such evidence suggests that impaired recognition of TBF items in the study by Ullsperger and colleagues might have been exacerbated by retrieval of the TBR items following each test block beyond the detrimental influence of the forget-instruction cues presented during study. Accordingly, the fact that our participants were not given a similar opportunity to selectively recall the TBR items (consistent with most directed-forgetting experiments) could explain the absence of a late right-frontal positivity associated with release from inhibition. Indeed, such late frontal positivity was also not observed by Nowicka et al. (2009) and Paz-Caballero and Menor (1999).

1 In the study by Ullsperger et al. (2000), effects of a directed-forgetting manipulation were compared to those of a depth-of-processing manipulation. In this latter condition, the task between test blocks was to count aloud backwards for 60 s. It could be argued that this is fundamentally different from recalling a subset of the preceding study words. Moreover, the effect of depth-of-processing on recognition accuracy was markedly smaller than that of directed forgetting, primarily due to a relatively higher number of hits for shallowly encoded words than TBF words. This supports our argument that the interpolated task of recalling a subset of studied words in the DF task (but not the depth-of-processing task) was instrumental in producing ERP evidence of inhibition.

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4.3. Conclusions and directions for future research In conclusion, our study of item-cued directed forgetting produced electrophysiological evidence consistent with notions of memory inhibition that were manifested in both lexical decisions (indirect memory test) and recognition-memory judgements (direct memory test). Replicating a recent study by Nowicka et al. (2009), we observed a reversed old/new effect for TBF items that were successfully forgotten, suggesting that instructions to forget might inhibit the return of attention to these items at time of retrieval. Extending their investigation, we also demonstrated that forgotten TBF items elicited relatively enhanced early (150– 250 ms) and late (800–1000 ms) negativities in a lexical-decision task, implicating that inhibitory influences not only affect conscious recollection processes but rather produce general suppression of participants’ memory representations of unwanted information. Clearly, it would be beneficial for future research to examine ERPs during retrieval of TBR words that are unintentionally forgotten as a means of comparing the consequences of active vs. passive forgetting. In the current study this was not possible due to the relatively high recognition accuracy for TBR items. In a study that examined fMRI data from the study phase as a function of subsequent behavioural outcomes (i.e., TBR-r, TBR-f, TBF-r, and TBF-f), Wylie, Foxe, and Taylor (2008) demonstrated that intentional forgetting engaged frontal structures that were not active during unintentional forgetting. As an extension of this investigation, it would be interesting to combine these results with those obtained during the test phase to more fully evaluate the relations between encoding and retrieval processes. Furthermore, in light of our suggestion that directed forgetting instructions suppress memory representations in general, their potential detrimental effects on other processes than conscious recollection in direct memory tasks need to be investigated more systematically, and in this context, singleprocess models of recognition memory (e.g., Wixted, 2007) should also be considered. Similar to a study by Spitzer and Bäuml (2007), which examined inhibitory influences as a result of retrieval-induced forgetting, this could be achieved, for example, by incorporating the remember-know procedure or by including confidence ratings from which ROC curves could be calculated. Finally, it would be desirable to study other kinds of indirect memory tasks to test our conclusion that inhibition affects memory representations in general rather than conscious recollection in particular. This could be combined with different repeated-measures designs to fully evaluate the conditions under which inhibition either is or is not dissipated by re-exposure of TBF items. Acknowledgments This project was supported by a Promising Researcher Grant from University of Kent. We would like to thank Elizabeth Sargeant for help with data collection and Keith Franklin for programming support. We are also grateful to Dr. Axel Mecklinger and three anonymous reviewers for their constructive and helpful comments on an earlier version of this paper.

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