Elaborately rehearsed information can be forgotten: A new paradigm to investigate directed forgetting

Journal Pre-Proof Elaborately Rehearsed Information Can be Forgotten: A New Paradigm to Investigate Directed Forgetting Heming Gao, Mingming Qi, Qi Zhang PII: DOI: Reference:

S1074-7427(19)30130-3 https://doi.org/10.1016/j.nlm.2019.107063 YNLME 107063

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Neurobiology of Learning and Memory

Received Date: Revised Date: Accepted Date:

2 July 2018 24 July 2019 30 July 2019

Please cite this article as: Gao, H., Qi, M., Zhang, Q., Elaborately Rehearsed Information Can be Forgotten: A New Paradigm to Investigate Directed Forgetting, Neurobiology of Learning and Memory (2019), doi: https://doi.org/ 10.1016/j.nlm.2019.107063

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Elaborately Rehearsed Information Can be Forgotten: A New

School of Psychology, Liaoning Normal University, Dalian, 116029, China.

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Heming Gao1*, Mingming Qi1*, Qi Zhang1

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Paradigm to Investigate Directed Forgetting

*Correspondence should be addressed to Heming Gao, School of Psychology, Liaoning

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Normal University, Dalian, 116029, China. E-mail: [email protected], and Mingming Qi, School of Psychology, Liaoning Normal University, Dalian, 116029,

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China. E-mail: [email protected].

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JOURNAL PRE-PROOF Abstract In previous item-method directed forgetting (DF) studies, forgetting may have occurred when the maintenance rehearsal of memory items was performed. In this study, a modified item-method DF paradigm was adopted to investigate whether forgetting

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instruction could produce a positive effect on forgetting the items that were elaborately

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rehearsed. During the study phase, a to-be-forgotten (TBF) word was followed by a

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forgetting cue. If no cue followed, the word was a to-be-remembered (TBR) item.

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Participants were required to intentionally memorize the word when it appeared. During the test phase, a yes/no recognition (Experiment 1) or a remember/know procedure

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(Experiment 2) was adopted. The behavioural results revealed that both the hit rate (Experiment 1) and remembering rate (Experiment 2) were higher for TBR relative to

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TBF words. For correctly identified old words, reaction times were consistently shorter for TBR compared to TBF words. These results revealed superior memory retention for

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TBR than for TBF words. The event-related potential (ERP) results revealed that, during both FN400 and late-positive complex (LPC) time windows, the remembered

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TBR words evoked more positive ERPs than the remembered TBF words and correctly rejected (CR) words (i.e., FN400 and LPC old/new effects). However, more negative

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ERPs were evoked for both remembered and forgotten TBF words than for CR words

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during the LPC time window (i.e., reversed LPC old/new effect). These results demonstrated that TBF words were associated with lower level of familiarity and recollection process than TBR words. The memory representation of TBF information might be inhibited. Key words: Intentional forgetting; Memory inhibition; FN400; LPC; Old/new effect

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1. Introduction Directed forgetting (DF) refers to the memory damage caused by forgetting instructions. Previous studies have adopted an item-method DF paradigm to investigate

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the intentional forgetting phenomenon (Anderson & Hanslmayr, 2014; Marks &

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Dulaney, 2001; Wylie, Foxe, & Taylor, 2008). During the study phase, items were

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randomly followed by a remembering or forgetting cue. If a remembering cue was

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presented, the item was considered to-be-remembered (TBR), and if a forgetting cue was presented, the item was considered to-be-forgotten (TBF). Numerous studies have

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demonstrated that TBF items are associated with worse memory retention than TBR

& Muller, 2000).

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items during the test phase, indicating a DF effect (Paller, 1990; Ullsperger, Mecklinger,

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The selective rehearsal hypothesis suggests that the DF effect is due to a more

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intensive encoding effort for TBR items than for TBF items after presentation of the respective cues (Basden, Basden, & Gargano, 1993). Several ERP studies have found

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that, during the 200–800 ms time window, remembering cues evoke more positive

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ERPs than forgetting cues over the parietal scalp (Bailey & Chapman, 2012; Paller, 1990; Paz-Caballero, Menor, & Jimlnez, 2004). Additionally, some researchers (Gao et al., 2016a, b; Yang et al., 2012; Patrick, Kiang, & Christensen, 2015) found that remembering cue evoked a larger parietal P3 component compared to the forgetting cue. These studies suggested that remembering cue evoked a more intensive rehearsal process for the TBR items. In addition, some studies have found that cues associated with correctly recognized items evoke more positive ERPs than those associated with 3

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incorrectly rejected items. This ERP subsequent memory effect was enhanced for TBR compared with TBF items, suggesting better recognition of TBR items (Hauswald, Schulz, Iordanov, & Kissler, 2010; Hsieh, Hung, Tzeng, Lee, & Cheng, 2009; Schindler

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& Kissler, 2018; Van Hooff & Ford, 2011).

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The attentional inhibition hypothesis suggests that forgetting cues trigger an

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inhibitory process to prevent TBF information from being further processed, and/or

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suppress the memory representation of TBF information to sub-baseline levels (Zacks & Hasher, 1994; Zacks, Radvansky, & Hasher, 1996). Some electrophysiological

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studies found forgetting cues evoked more positive ERPs than remembering cues over

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the frontal scalp (Gallant & Dyson, 2016; Gao, Qi, & Zhang, 2018; Hauswald et al., 2010; Ludowig et al., 2010; Paz-Caballero et al., 2004), and some studies found the

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forgetting cue evoked a larger frontal N2 component compared to the remembering cue (Gao et al., 2016a; Patrick, Kiang, & Christensen, 2015; Yang et al., 2012). These

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results suggested that the item-method DF engaged an active frontal inhibition process.

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Recognition is supported by separate processes of recollection and familiarity

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(Dual-process models of recognition memory; Yonelinas, 2002). Recollection refers to as a recall-like process that retrieves detailed memories about individual items or episodes. Familiarity has been referred to as a memory process that supports recognition without the detailed information that is characteristic of recollection (Diana, Vilberg, & Reder, 2005; Gardiner, Gawlik, & Richardson-Klavehn, 1994). Previous recognition studies (Allan, Wilding, & Rugg, 1998; Duzel, Yonelinas, Mangun, Heinze, & Tulving, 1997; Mecklinger, 2000) have found that the 4

old items evoked

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more positive ERPs relative to the

new words, and this phenomenon

was termed as ERP old/new effect. Based on the temporal and topographical distributions, the frontal N400 (FN400) old/new effect and parietal LPC old/new effect

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were distinguished. The FN400 old/new effect was maximally distributed over the

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frontal scalp during the 300–500 ms time window, which has been associated with the

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familiarity level in the recognition process. The parietal old/new effect was maximally

related to the conscious recollection process.

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distributed over the parietal scalp during the 500–800 ms time window, which has been

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Ullsperger et al. (2000) initially investigated the ERP old/new effects in DF studies

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and found that TBR items evoked both FN400 and parietal old/new effects. However, TBF items evoked only an FN400 old/new effect. These results were replicated by the

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following studies (Nowicka et al., 2011; Van Hooff & Ford, 2011). Moreover, it was found that the subsequently forgotten TBF items evoked more negative ERPs than the

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CR items during the LPC time window (i.e., reversed old/new effect; Nowicka et al., 2011; Van Hooff & Ford, 2011). These results suggested that TBF items might be

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inhibited and were thus more difficult to retrieve. Some researchers have suggested that inhibition is not the main determinant of the

DF effect. The frontal activation during intentional forgetting of TBF information might be associated with preparatory information-filtering processes (Bastin et al., 2012) or other non-inhibitory processes, such as attention orienting and conflict monitoring (Zwissler, Schindler, Fischer, Plewnia, & Kissler, 2015). The effectiveness of forgetting cues in the typical item-method DF paradigm has also been challenged. There is 5

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growing evidence that forgetting cues play a small role in forgetting items. Some studies have reported that memory performance for TBF items improves with increased cue duration (Bancroft, Hockley, & Farquhar, 2013; Lee, Lee, & Tsai, 2007).

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Recently, several studies (Gao et al., 2016b; Gao, Qi, Zhang, in press; Schindler

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& Kissler, 2018; Zwissler et al., 2015) have also demonstrated that compared to a no-

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cue (NC) or uncued (UI) control condition in which the items were assumed to be

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incidentally encoded, forgetting cues surprisingly improve the memory retention of TBF items. This suggests that the TBF items were processed further after the

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presentation of forgetting cues, and that the memory representation of TBF items was

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not suppressed or inhibited to sub-baseline levels.

In the typical item-method DF paradigm, memory for the items might be retained

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with minimal cognitive effort until the cues were presented (i.e., wait-and-see strategy);

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only if a remembering cue was presented, the item was elaborately rehearsed (Bancroft et al., 2013; Basden et al., 1993; Hourihan & Taylor, 2006). Some researchers suggested

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that the item-based directed forgetting procedure was not truly directed forgetting, but

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rather a manipulation of intention to learn (Bancroft et al., 2013; Johnson, 1994). Due to the wait-and-see strategy, participants were discouraged to intentionally memorize the items before the cues are presented (i.e., incidental learning). This view was supported by the finding that participants had superior memory of the TBR items, which were assumed to be recalled through elaborate rehearsal after the presentation of remembering cues, than the NC/UI items, which were assumed to be encoded incidentally (Gao et al., 2016b; Gao et al., in press; Schindler & Kissler, 2018; Zwissler 6

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et al., 2015). The role of forgetting cues in item-method DF procedure might be terminating or reducing the maintenance rehearsal process for TBF items. Hourihan and Taylor (2006) suggested that the typical item-method task did not

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provide an effective model for DF in the real world (i.e., forgetting in the context of

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intentional remembering). In addition, such a model did not adequately capture the

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cognitive control processes normally at work during intentional forgetting. They

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designed a modified item-method DF paradigm to investigate whether the forgetting cues could stop the elaborate encoding process. Specifically, if a cue was presented, the

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word was a TBF item, and if no cue followed, the word was a TBR item. Hence,

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participants were required to intentionally memorize the word when it appeared. In other words, an instruction to forget was given following an intention to remember. By

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contrast, in item-method DF paradigm, an instruction to forget was given following an intention to perform maintenance rehearsal. In their Experiment 1, the forgetting cues

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were presented for 1 s. The post-word blank interval was always longer for the remembering (i.e., 11 s) relative to the forgetting (0, 5, or 10 s) trials. A DF effect was

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observed, and the memory performance improved with prolonged word-cue interval.

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This finding indicated that forgetting cues can stop the remembering process, and that earlier presentation of a forgetting cue is more likely to stop the encoding process. The superior memory performance for TBR words relative to TBF words might be the result of the additional rehearsal time provided for TBR words (Hourihan & Taylor, 2006). In their Experiment 2, the authors reduced this effect by adjusting the post-word blank interval for TBR trials to be equally long as the interval following the 7

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post-word blank onset time and cues offset time for TBF trials. In other words, the postword blank interval was longer for the remembering than the forgetting trials. Therefore, the superior memory performance for TBR words might also be due to the longer

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rehearsal time (i.e., duration of the forgetting cue). The inferior memory performance

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for TBF words compared to TBR words suggested that the encoding process of TBF

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could be terminated; however, when compared with the decay of memory traces, it

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remains unclear whether forgetting cues could promote the DF effect.

This study aimed to investigate whether the forgetting cues could help people to

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forget more items that were asked to be elaborately rehearsed. In this study, we modified

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the paradigm adopted by Hourihan and Taylor (2006). Specifically, no remembering cues were presented for TBR words and forgetting cues were presented to indicate TBF

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words. In the TBR condition, the duration of exposure to the blank screen, which followed the words, was equal to the inter-stimulus interval between the words and cues

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in the TBF condition (Figure 1). In other words, when compared to the TBR condition, an additional forgetting cue was presented in the TBF condition. The differential

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memory performance between the TBR and TBF conditions might be due to the

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prolonged cognitive processing triggered by the forgetting cue. We hypothesized that if forgetting cues negatively affected the processing of TBF

words, there would be superior memory performance for the TBR words compared to the TBF words. Accordingly, the pronounced FN400 old/new effect which is often associated with familiarity, and the parietal old/new effect which is associated with the recollection process (Duzel et al., 1997; Jäger, Mecklinger, & Kipp, 2006; Rugg & 8

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Curran, 2007) would be expected for the correctly recognized TBR words than for the recognized TBF words. In contrast, better memory retention for the TBF words than for the TBR words would support the view that forgetting cues cannot prevent items

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from further processing. Therefore, reduced FN400 and LPC old/new effects would be

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expected for TBR words compared to TBF words.

2.1 Experiment 1

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2.1.1 Participants

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Thirty-five native Chinese-speaking undergraduate students were recruited for this study. Four participants were excluded due to excessive artifacts during

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electroencephalography (EEG) recordings (more than 50% of their trials per condition were invalid). Therefore, data from 31 participants were included in the analyses (18

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men and 13 women, mean age ± standard deviation = 22.1 ± 2.28 years). All participants were healthy and right-handed and had normal or corrected-to-normal

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eyesight. None of the participants was colour-blind.

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This study was approved by the Research Ethics Committee of Liaoning Normal

University of China, and was conducted in accordance with the ethical guidelines of the Declaration of Helsinki. All participants provided their written informed consent and were monetarily compensated upon completion of the experiment. 2.1.2 Design and materials

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A one-factor, within-subject design was adopted. Two conditions were included in the study phase: TBR and TBF. The order of experimental trials was pseudorandomised with the constraint that no more than three consecutive trials could be from

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the same cue condition. Participants were informed that words followed by red Xs were

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TBF items and that memory for these words would not be tested. In contrast, words not

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followed by an explicit cue were TBR items, and memory for these words would be

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tested. Participants were informed that because no cues followed the TBR words, to remember more TBR words, it was important to try to commit words to memory at the

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word onset.

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The stimuli were Chinese double-character nouns selected from the top 8,000 words in ‘The Modern Chinese Frequency Dictionary’, with a mean frequency of 7.388

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per thousand, and a mean strokes of 16.82. The words were allocated to four lists of 60 words. Each list was matched for mean number of strokes (ps > 0.891) and frequency

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(ps > 0.877). Two lists were used as study items, and the remaining two lists served as new words (distractors) during the test phase. Two additional buffer words (no cues

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were followed) that were excluded from subsequent analyses were presented at the

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beginning and end of the task. With the exception of these two buffer words, the study phase consisted of 120 trials (60 trials per condition) and the test phase consisted of 240 trials. The order of presentation for each of the lists was counterbalanced across participants. The participants received a short break (30 s) after each set of 60 trials. Following the study phase, the participants were instructed to count backwards from 100 in 10

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multiples of 3. They were then offered a break of approximately 5 minutes before the test phase. In the test phase, participants were instructed to provide the response “old” to the

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words that had appeared in the study phase, regardless of whether they had been

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instructed to remember or forget these words. They were instructed to respond with the

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term “new” to the words that had not been presented during the study phase.

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Participants were told that there was no fixed order for the presentation of the stimuli. Furthermore, the number of old/new words was randomly assigned by the computer;

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hence, the ratio might not be 1:1. Participants were instructed to respond realistically.

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2.1.3 Procedure

During the study phase, each trial started with the presentation of a fixation cross

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for 500 ms, followed by a blank screen for 500 ms. Subsequently, each word was presented for 1,000 ms. For the TBR condition, the trial ended with a 2,000-ms

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presentation of a blank screen. However, for the TBF condition, after the 2,000-ms blank screen presentation, the trial ended with a forgetting cue, presented for 1,000 ms

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(Figure 1a).

-------------------------------------------------Insert Figure 1 about here ---------------------------------------------------

During the test phase, a 500-ms fixation cross was presented, followed by a random blank screen for 500–800 ms. A word was then presented for 1,500 ms. Finally, 11

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a blank screen was presented for 1000 ms (Figure 1b). The participants were instructed to press “F” or “J” on the keyboard to indicate ‘old’ or ‘new’ as their responses to the word presentation, respectively, as quickly and accurately as possible.

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2.1.4 Data analysis

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(1) Behavioural data analysis

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Reaction time (RT) was defined as the time between the test word onset and the

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key press. Based on memory cue and behavioural response combinations, RT data were sorted into six experimental conditions: TBR-R and TBR-F (remembered and forgotten

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TBR), TBF-R and TBF-F (remembered and forgotten TBF), FA (false alarm, new items

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that were made old responses) and CR (correctly rejected) items. Preliminary data inspection indicated that the hit rate for each word type was higher

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than the false alarm rate (ts > 13.31, ps < 0.001). Then, a paired sample t-test was performed on the hit rates. A 2 (Response Type: remembered, forgotten) × 2 (Word

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Type: TBR, TBF) repeated-measures ANOVA was conducted for the RT data.

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(2) ERP recording and analysis

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Brain electrophysiological activity was recorded from a 64-channel EEG recording

system (Brain Products GmbH, Gilching, Germany) with references on a central midline electrode. A vertical electrooculogram (EOG) signal was recorded using electrodes placed below the right eye. A horizontal EOG signal was recorded using electrodes placed on the right canthi. All interelectrode impedances were maintained below 5 kΩ. The EEG and EOG signals were amplified using a 0.05–100-Hz band pass filter and continuously sampled at 500 Hz for off-line analysis. 12

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Raw EEG data were processed offline using BrainVision Analyzer version 2.1 (Brain Products GmbH). For data analysis, ERPs time-locked to word onset during the test phase were re-referenced to the average values at the left and right mastoids. After

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ocular correction using independent component analysis algorithms, EEG signals were

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digitally filtered using a 35-Hz low-pass filter with a 24-bit analogue-to-digital

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converter. The ERP signals for all words during the test phase were then segmented into

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1,000-ms epochs surrounding stimulus presentation and baseline-corrected with respect to the 200 ms pre-stimulus. Trials contaminated with EOG artifacts (mean EOG voltage

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exceeding ±80 μV) and those with artifacts due to amplifier clipping, bursts of

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electromyographic activity, or peak-to-peak deflections exceeding ±100 μV were excluded from averaging. The EEG signals recorded in all conditions were averaged

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separately for each participant.

For the ERPs evoked by the words during the test phase, the FN400 (300–500 ms)

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and LPC (500–800 ms) time windows were selected for statistical analysis. These time periods corresponded to the typical latency ranges of the FN400 and LPC components,

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respectively (Mecklinger, 2000). Based on the grand averaged and topographical ERP

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maps (Figure 3), 12 electrodes were selected for statistical analysis. These electrodes were placed over six scalp regions (left-frontal: F1 and F3; right-frontal: F2 and F4; left-central: C1 and C3; right-central: C2 and C4; left-parietal: P1 and P3; and rightparietal: P2 and P4), and mean amplitudes were computed over pairs of electrode sites. Repeated-measures ANOVAs with word type [TBR-R, TBF-R, TBF-F and correctly rejected (CR)], caudality (frontal, central, and parietal), and hemisphere (left and right) 13

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as within-subject factors were performed on the mean amplitudes of the FN400 and LPC components. The means of individual ERP trials per condition per subject were as follows: TBR-

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R, 28.8; TBF-R, 34.3; TBF-F, 26.3 and CR, 85.7. Because no sufficient mean ERP trials

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were obtained for TBR-F words (17.6), the ERPs evoked by TBR-R words were not

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included in the formal analysis. To avoid describing large amounts of statistical data

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concerning scalp distribution effects, only the main effects or interactions that included the word type factor have been reported. All effects with more than one degree of

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freedom were adjusted for sphericity violations using the Greenhouse-Geisser

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correction. 2.1.5 Results

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2.1.5.1 Behavioural results

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As shown in Figure 2a, recognition accuracy was 66.4% for TBR words, and 51.3% for TBF words. The FA rate was 22.2% for new items. The results showed that the hit

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rate was higher for TBR words than for TBF words [t(30) = 6.28, p < 0.001, d = 1.218,

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1-β = 0.998]. The mean RTs were 780.6 ms for TBR-R words, 816.4 ms for TBF-R words, 820

ms for TBR-F words and 827 ms for TBF-F words (Figure 2b). The ANOVA revealed a significant Response Type × Word Type interaction [F (1, 30) = 5.02, p = 0.033, ηp2 = 0.143, 1-β = 0.769]. Simple effect analysis revealed that the RTs were shorter for remembered compared with forgotten responses for TBR words (p = 0.028), this RT 14

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difference was not found for TBF words (p = 0.513); RTs were shorter for TBR-R words than for TBF-R words (p < 0.001); no RT difference was found between TBR-F and

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Insert Figure 2 about here

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--------------------------------------------------

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TBF-F words (p = 0.566).

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--------------------------------------------------2.1.5.2 ERP results

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During the FN400 (300–500 ms) time window, the Word type × Hemisphere

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interaction was significant [F(3, 90) = 5.02, p = 0.003, ηp2 = 0.143, 1-β = 0.905]. Simple effect analysis revealed that less negative ERPs were evoked for TBR-R words than for

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TBF-R words over both left (p = 0.020) and right hemispheres (p = 0.002); TBR-R words evoked less negative ERPs than TBF-F words over both left (p = 0.003) and right

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hemispheres (p = 0.048); TBR-R words evoked less negative ERPs than CR words over the left hemisphere (p = 0.016), and this ERP difference reached marginally significant

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over the right hemisphere (p = 0.059); no ERP differences were found among TBF-R,

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TBF-F and CR words over both left and right hemispheres, ps > 0.116 (Figure 3). -------------------------------------------------Insert Figure 3 about here --------------------------------------------------During the LPC (500–800 ms) time window, the Word type × Caudality × 15

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Hemisphere interaction was significant [F(6, 180) = 3.175, p = 0.006, ηp2 = 0.096, 1-β = 0.917]. Simple effect analysis revealed that TBR-R words evoked more positive ERPs than TBF-R words over all scalps, ps < 0.014; TBR-R words evoked more positive

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ERPs than TBF-F words over the left-frontal, left-central, left-parietal, and right-

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parietal scalps, ps < 0.013; TBR-R words evoked more positive ERPs than CR words

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over the left-parietal scalp (p = 0.042) and right-parietal scalp (p = 0.007); TBF-R words

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evoked more positive ERPs than TBF-F words over the left-central scalp, p = 0.048; TBF-R words evoked more negative ERPs than CR words over right-frontal (p = 0.029)

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and right-central (p = 0.025) scalps; TBF-F words evoked more negative ERPs than CR

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words over left-frontal, right-frontal, left-central and left parietal scalps, ps < 0.024. 2.1.5.3 Correlational analyses

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To better determine the functional means of observed ERP effects, Pearson

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correlation analysis was performed to investigate the association between the hit rates and the amplitudes of the FN400 and LPC components. The amplitudes of the FN400

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component were calculated by averaging the amplitudes from four frontal electrodes

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(i.e., F1, F3, F2, F4), as well as from four parietal electrodes (i.e., P1, P3, P2, P4) for the LPC amplitudes. The results showed that, for the TBR words, a positive correlation was found

between the hit rates and the LPC amplitudes, r = 0.422, p = 0.018. No correlation was found between the hit rate and the FN400 amplitudes, r = 0.06, p = 0.731. For the TBF items, a positive correlation was found between the hit rate and the FN400 amplitudes,

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r = 0.364, p = 0.044. No correlation was found between the hit rate and the LPC amplitudes, r = 0.269, p = 0.134. 2.1.6 Discussion

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The behavioural results indicated superior hit rates for TBR words compared to

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TBF words. This might indicate that TBR words were better encoded than TBF words.

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In addition, shorter recognition RTs were observed for TBR-R words than for TBF-R

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words. Previous studies on recognition memory have suggested that deeper memory traces and greater degrees of familiarity lead to shorter recognition RTs (Henson, Rugg,

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Shallice, & Dolan, 2000; McDonough, Wong, & Gallo, 2013; Shanks & Perruchet,

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2002). The shorter recognition RTs for the TBR-R than for the TBF-R words might further indicate that the TBR-R words exhibited superior memory retention than the

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TBF-R words. In addition, RTs were longer for TBR-F relative to TBR-R words, indicating a lower confidence in judging TBR words as new ones. In contrast, no RT

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differences were found between TBF-F and TBF-R words, indicating similar low

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response confidence in judging TBF words compared to TBR words.

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The ERP results indicated that, during the FN400 time window, less negative ERPs

were evoked for the TBR-R words than for the CR words over the whole scalp, with areas of maximum difference distributed over the left hemisphere (Figure 3). This was in line with the findings of previous DF studies (Nowicka, Jednorqg, Wypych, & Marchewka, 2009; Ullsperger et al., 2000; Van Hooff, Whitaker, & Ford, 2009). In contrast, no ERP differences were found between TBF-R/TBF-F and CR words. These results indicated that the FN400 old/new effect was observed for the TBR words, but 17

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not for the TBF words. In addition, the FN400 amplitudes were more negative for TBFR/TBF-F words compared to TBR-R words. Previous studies have demonstrated that FN400 amplitude is more negative when items are less familiar (Diana et al. 2005; D¾

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zel et al., 1997), and that the left-lateralized FN400 old/new effect is associated with

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word familiarity during recognition judgement (Jäger et al., 2006; Rugg & Curran,

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2007). Accordingly, the reduced FN400 amplitude and old/new effect for TBF words

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compared to TBR words might reflect a lower degree of familiarity with the TBF words during the recognition judgement. In previous DF studies (Nowicka et al., 2009;

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Ullsperger et al., 2000; Van Hooff et al., 2009), the FN400 old/new effect was also

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found for TBF words. However, it was not observed for the TBF words in this study. This finding further supported the view that the TBF words in this study had lower

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degrees of familiarity than the TBR words.

During the LPC time window, the ERPs were more positive for the TBR-R words

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than for the TBF-R/TBF-F words. The LPC activity might reflect memory trace strength, with more positive LPC amplitudes for increasing memory trace strengths

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(Olichney et al., 2000; Paller, Kutas, & McIsaac, 1995; Van Strien, Hagenbeek, Stam,

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Rombouts, & Barkhof, 2005). In this study, the enhanced LPC activity for the TBR-R words compared to the TBF-R/TBF-F words might indicate greater memory trace strength for the TBR-R words. More positive ERPs were evoked for the TBR-R words than for the CR words (i.e., LPC old/new effect) over the parietal scalp. However, more negative ERPs were evoked for the TBF-R/TBF-F words than for the CR words over the right fronto-central scalps. 18

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This effect has been termed as the reversed old/new effect (Nowicka et al., 2009). The LPC old/new effect was assumed to reflect recollection processes (Jäger et al., 2006; Rugg & Curran, 2007). Therefore, the pronounced LPC old/new effect for the TBR

F

words compared to TBF words might suggest a more effortful retrieval process for the

O

TBR words.

O

Finnigan, Humphreys, Dennis, and Geffen (2002) have suggested that the

PR

amplitude of the late positive complex (LPC) effect is sensitive to decision accuracy (and perhaps confidence) and the amplitude is greater with higher confidence. Previous

E-

studies (Nowicka et al., 2009; Van Hooff et al., 2009) have found a reversed old/new

PR

effect for forgotten TBF words. This reversed effect was thought to reflect the participant's lack of confidence regarding the familiarity of the forgotten TBF words

AL

during the study phase. In our previous study (Gao et al., 2016b), the right-lateralized reversed old/new effect was also thought to be associated with decision confidence.

R N

Accordingly, the pronounced reversed old/new effect might reflect lower confidence in recognition judgment. In short, in this study, the TBF-R/TBF-F words might have been

U

associated with a lower level of familiarity and conscious recollection than the TBR-R

JO

words.

The significant positive correlation between hit rates and the LPC amplitudes for

TBR words indicated that the recognition response for the TBR words was based more on recollection than on familiarity. This result was in line with the findings of previous DF studies, which showed that enhanced LPC/P3 activity was positively correlated with higher subsequent memory performance (Patrick et al., 2015; Gao et al., 2018). 19

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However, for the TBF words, the hit rates were correlated with the FN400 amplitudes but not with the LPC amplitudes, indicating that the recognition response for TBF items was based more on familiarity than on recollection.

F

TBF-R words evoked more negative ERPs than CR words over the right fronto-

O

central scalps, in addition, the TBF-F words also evoked a more pronounced reversed

O

LPC old/new effect than the TBF-R words. These results might suggest lower

PR

confidence in judging of an TBF word as a new relative to an old one. This interpretation was also supported by the RT results which have shown longer RTs for

E-

TBF-F relative to TBF-R items. Nowicka et al. (2009) suggested that the reversed

PR

old/new effect seems to reflect intentional and effective inhibition to TBF items. According to this view, the pronounced reversed LPC old/new effect for TBF-F relative

AL

to TBF-R words might reflect a more intensive inhibition process for TBF-F words. The neural differences between TBR-R and TBR-F words were expected to be different

R N

from those between TBF-R and TBF-F words. Because no sufficient mean ERP trials were obtained for TBR-F words, future studies could adopt other techniques (e.g., fMRI)

JO

U

or increase the number of TBR words to address this issue.

2.2 Experiment 2 Previous studies (Diana et al., 2005; D¾zel et al., 1997) have demonstrated that FN400 amplitude is more negative when items are less familiar. D¾zel et al. (1997) have demonstrated that the FN400 is associated with knowing responses in the

20

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remember/know paradigm, and the parietal old/new effect is of greatest magnitude in the remember/know paradigm when a remembering response is made. Gardiner et al. (1994) investigated the influence of the DF on recollection and familiarity. Specifically,

F

in the test phase, participants were asked to make remember or know responses to

O

indicate whether recognition of each word was accompanied by conscious recollection

O

or by feelings of familiarity in the absence of conscious recollection. They found the

PR

remembering rate was higher for TBR relative to that for TBF items, but no knowing rate differences were found between them. In other words, the remember-versus-forget

E-

designation influenced the participants’ ability to remember but not their ability to the

PR

know responses.

In DF studies, remembering cues evoked elaborate rehearsal process for the TBR

AL

words, which was absent for forgetting cues. By contrast, the forgetting cues might be served as hints to cease the maintenance rehearsal process. Gardiner et al. (1994)

R N

suggested that remembering response depended on elaborative rehearsal, and knowing response depended on maintenance rehearsal. To further investigate the influence of the

U

DF on recollection and familiarity of elaborately rehearsed items, a remember/know

JO

procedure was adopted in the Experiment 2. 2.2.1 Participants A set of 30 participants (different from the participants in Experiment 1) completed this study. The data from 3 participants were excluded from the analysis due to the participants’ failure to comply with the task instructions. Therefore, data from 27

21

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participants were included in the analyses (10 men and 17 women, mean age = 22.2 years, SD = 2.71). All participants were healthy and right-handed and had normal or corrected-to-normal eyesight. None of the participants was colour-blind. This study was

F

approved by the Research Ethics Committee of Liaoning Normal University of China,

O

and was conducted in accordance with the ethical guidelines of the Declaration of

PR

compensated upon completion of the experiment.

O

Helsinki. All participants provided their written informed consent and were monetarily

E-

2.2.2 Design and materials

Design and materials were identical to those described for Experiment 1, with the

PR

exception that the remember/know procedure was adopted during the test phase. During the test phase, the participants were told to press the “1” key if the

AL

recognition of the word was accompanied by a conscious recollection of the word's

R N

occurrence in the study list. If recognition of the word was accompanied by a sensation that the word had occurred in the study list but without a recollection of its occurrence,

U

they were instructed to press the “2” key. Finally, if a word was not previously seen in

JO

the experiment, participants were instructed to press the “3” key. The participants were given detailed instructions, similar to those used in previous studies (Basden, 1996; Gardiner et al., 1994). 2.2.3 Procedure Procedure was identical to the one used in Experiment 1. 2.2.4 Data analysis 22

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Three response types were obtained for each word type, i.e., remembering, knowing, and new. Recognition proportion rate was defined as the percentage of response type in each word type condition. Reaction time (RT) was defined as the time

F

between test word onset and the key press. Based on memory cue and behavioural

O

response combinations, RT data were sorted into four experimental conditions: r-TBR,

O

k-TBR (remembered and known TBR), r-TBF, and k-TBF (remembered and known

PR

TBF).

Preliminary inspection of the data indicated that, for both TBR and TBF words,

E-

the sum of the remembering rate and knowing rate was higher than the false alarm rate

PR

(29.2%), ts > 11.31, ps < 0.001. Then, a 2 (Response Type: remembering, knowing) × 2 (Word Type: TBR, TBF) repeated-measures ANOVA was conducted on the

AL

recognition proportion rates. A 2 (Response Type: remembering, knowing) × 2 (Word Type: TBR, TBF) repeated-measures ANOVA was conducted on the recognition RTs.

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2.2.5 Results

U

As shown in Figure 4a, remembering rate was 51.6% for TBR words and 36.1%

JO

for TBF words, while knowing rate was 20.4% for TBR words and 24.9 % for TBF words. For the recognition proportion rate, the ANOVA revealed a significant Response Type × Word Type interaction [F (1, 26) = 33.49, p < 0.001, ηp2 = 0.563, 1-β = 0.995].

Simple effect analysis revealed that the remembering rate was higher for TBR words relative to TBF words, p < 0.001; the knowing rate was lower for TBR words relative to TBF words, p < 0.001; and the remembering rate was higher than knowing rate for both TBR and TBF rates, ps < 0.037. 23

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-------------------------------------------------Insert Figure 4 about here

F

---------------------------------------------------

O

For the RT data, a significant main effect of word type was observed [F (1, 26) =

O

6.09, p = 0.021, ηp2 = 0.563, 1-β = 0.661], with longer RTs for TBF compared to TBR

PR

words. The main effect of response type was significant [F (1, 26) = 36.99, p < 0.001, ηp2 = 0.587, 1-β = 0.999], with longer RTs for knowing than remembering responses.

E-

2.2.6 Discussion

PR

Compared to the TBF words, higher proportion of remembering responses was made for the TBR words. During the studying phase, same post-word blank intervals

AL

were presented for different words. The remembering rate differences between conditions might be attributed to the effect of forgetting cues. Some studies (Basden,

R N

1996; Gardiner et al., 1994) suggested that remembering depended on an elaborative rehearsal, reflecting the conscious recollection process. The reduced remembering rate

U

suggested that the memory representation of TBF words might be inhibited compared

JO

to the representation of TBR words, leading to a decrease in conscious recollection. Lower proportion of knowing responses were made for TBR words relative to TBF

words. Gardiner et al. (1994) suggested that the maintenance rehearsal process could increase the “know” responses. Some studies have suggested that participants process irrelevant information involuntarily if attentional resources are available (Lee et al., 2007; Lavie, 2005). Previous DF studies (Bancroft et al., 2013; Gao et al., 2016b; Lee 24

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et al., 2007; Schindler & Kissler, 2018; Zwissler et al., 2015) have demonstrated that forgetting cues cannot prevent words from being processed further. Forgetting cues instead triggered an additional rehearsal/encoding process for the TBF items (Schindler

F

& Kissler, 2018). In this study, one possibility is that TBF items might receive further

O

maintenance processing, leading to a higher knowing rate for TBF words relative to

O

TBR words.

PR

According to dual-process models of recognition memory, recollection is slower and more effortful than familiarity. However, Dewhurst, Holmes, Brandt, and Dean

E-

(2006) argued that participants’ experiences of remembering and knowing did not map

PR

directly onto the recollection and familiarity processes. Although familiarity is thought to be a faster process than recollection, Diana et al. (2005) suggested that the decision

AL

process (i.e., whether to accept an item based on its familiarity) could easily be delayed until after the completion of a recollection attempt and would result in slower RTs for

R N

knowing responses, compared to remembering responses. Therefore, in this study, the RTs for remembering trials were shorter than for knowing trials with both TBR and

U

TBF words. This was in line with the finding of Dewhurst et al. (2006), which also

JO

found remembering was faster than knowing responses. Previous studies (Schindler et al., 2018; Zwissler et al., 2014; Zwissler et al., 2015)

have found that the response criterion is different between TBR and TBF words. TBF words were responded to more conservatively than TBR words. Similarly, in this study, more knowing responses and less remembering responses were made for the TBR relative to the TBF words, suggesting that the response criterion might be different for 25

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different words. The RTs were shorter for TBR words than for TBF words in both remembering and knowing trials, likely because deeper memory traces and greater degrees of familiarity led to shorter recognition RTs (Henson et al., 2000; McDonough

F

et al., 2013; Shanks & Perruchet, 2002). It might also reflect participants’ requirement

O

for more mnemonic evidence to make an “old” decision for the TBF than for the TBR

O

words. These results might indicate that TBR words exhibited superior memory

E-

PR

retention than the TBF words.

PR

3. General Discussion

In this study, we aimed to investigate whether forgetting cues could exert negative effects on the memory retention of TBF items that were asked to be elaborately

AL

rehearsed. The results of both Experiments 1 and 2 have shown that TBR words have

R N

better memory retention than the TBF words. The ERP results of Experiment 1 indicated that TBR-R words evoked both FN400 and LPC old/new effects. In contrast,

U

these ERP old/new effects were absent for the TBF (both TBF-R and TBF-F) words.

JO

Instead, a reversed old/new effect was evoked, suggesting that TBR items showed higher levels of both familiarity and recollection processes compared to TBF items. This interpretation was consistent with the findings of Experiment 2. Forgetting cues led to a reduction in the remembering rate, which was assumed to be associated with the recollection process. Additionally, the RTs for r-TBR/k-TBR words were shorter than those for the r-TBF/k-TBF words, indicating a higher level of confidence in

26

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recognizing TBR compared to TBF words. Remembering response was associated with the recollection process, and knowing response was associated with the familiarity process (Basden, 1996; Gardiner et al., 1994). All these results suggested that TBR

F

words elicited more intensive familiarity and recollection processes compared to TBF

O

words.

O

In Experiment 2, for the TBR items, remembering rate was higher than knowing

PR

rate, and knowing rate was lower for TBR words than for TBF words. These results further supported the view that the recognition response for the TBR words was based

E-

more on recollection than on familiarity. Diana et al. (2005) suggested that the

PR

recognition decision process (i.e., whether to accept the item based on its familiarity) could easily be delayed until after the completion of a recollection attempt. The higher

AL

knowing rate for the TBF relative to the TBR words might also indicated recognition response for the TBF words were based more on familiarity than on recollection

R N

compared to the TBR words.

U

The hit rates to the TBR items found in this study (0.66 in Experiment 1 and 0.72

JO

in Experiment 2) were equivalent to those reported by other studies using the itemmethod paradigm (roughly 0.70, e.g., Gao et al., 2016b; Gardiner et al., 1994; Fawcett & Taylor, 2008; Van Hooff & Ford, 2011; Wylie et al., 2008). This finding might suggest that TBR items in this study were elaborately rehearsed as performed in the item-method DF paradigm. As introduced in the Introduction, some previous studies found superior memory performance for the TBF items than that for the NC/UI items (Gao et al., 2016b; Gao et al., in press; Schindler & Kissler, 2018; Zwisler et al., 2015). 27

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The memory retention for TBF words at the cue onset might be superior in the present study relative to the studies adopting the item-method DF paradigm. Due to the wait-and-see strategy in the typical item-method DF paradigm,

F

participants are discouraged from intentionally memorizing the items before the cues

O

are presented (incidental learning). The remembering/forgetting cues may serve as

O

triggers to deploy attention resources to items retained in the short-term memory and

PR

the TBF items might also receive involuntary rehearsal after the presentation of forgetting cues (Bancroft et al., 2013; Gao et al., 2016b; Lee et al., 2007; Schindler &

E-

Kissler, 2018; Zwissler et al., 2015). Therefore, forgetting cues are typically ineffective

PR

in promoting the forgetting effect for the incidental learning items. By contrast, in the present paradigm, the items were asked to be elaborately rehearsed before the

AL

presentation of forgetting cues. As mentioned in the Instruction section, when compared to the TBR condition, an additional forgetting cue was presented in the TBF

R N

condition. The differential memory performance between the TBR and TBF conditions might be due to the prolonged cognitive processing triggered by the forgetting cue. Both

U

the behavioural and electrophysiological results indicated an inferior memory retention

JO

for TBF items. Forgetting cues exerted a positive effect on the promotion of forgetting in this paradigm. Inhibition has been defined as the stopping or overriding of a mental process, in whole or in part, with or without intention (Mecloed, 2007). The role of inhibition in typical item-method DF paradigm involves attempts to suppress ongoing encoding, such that the participants can prevent awareness of the TBF items (Basden et al., 1993; 28

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Macleod, 1999). However, the TBF words will still be processed further in such cases (Bancroft et al., 2013; Gao et al., 2016b). By contrast, a reduction of hit rate or remembering rate for TBF words might suggest that the inhibition process in the present

F

paradigm suppressed the memory representation of TBF items and thus produced

O

complete and lasting amnesia for unwanted memories. However, on the basis of our

O

present findings, it was not possible to determine which stage of information processing

PR

was inhibited: encoding, retrieval, or both.

A growing number of researchers have adopted the typical item-method DF

E-

paradigm to investigate memory inhibition in both normal (Hauswald et al., 2010;

PR

Nowicka et al., 2011) and depressed participants (Berman et al. 2011; Kuehl et al., 2017; Yang et al., 2016). The frontal and parietal regions were activated during the forgetting

AL

of negative TBF items (Berman et al. 2011; Yang et al., 2016). Depressed individuals may experience greater difficulties in disengaging their attention from negative

R N

information. An alternative explanation for the frontal activation might be that more intensive attentional control processes, rather than the enhanced memory-inhibitory

U

processes, are triggered in response to the negative TBF information. Our findings

JO

highlight important avenues for future research. In particular, future studies could adopt the present paradigm to investigate the neural mechanisms underlying memory representation inhibition/suppression processes. Our study also provides an effective tool to investigate the phenomenon of memory suppression for both normal and clinical purposes.

29

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There were some limitations in this study. First, the participants were instructed to intentionally memorize the word when it appeared in this study. However, no specific strategies of the elaborate rehearsal were provided for the participants. Therefore, it was

F

unclear whether all the words were received deep processing. Previous studies

O

(Ullsperger et al., 2000; Rugg, Allan, & Birch, 2000) manipulated encoding depth by

O

cuing participants to process the word either deeply (e.g. sentence generation) or

PR

shallowly (alphabetic judgement tasks). Future studies are supposed to adopt this strategy to investigate the effectiveness of forgetting cues on promotion of forgetting

E-

the items that varied in encoding depth. Second, a previous study (Kwon, Nam, & Lee,

PR

2012) demonstrated that the recognition RTs and error rates increased when the stimulus words were orthographically similar to the higher frequency words. Although

AL

synonyms were excluded when selecting these words for this study, this neighbor effect should be eliminated in future studies. Third, because no cues were presented in the

R N

remembering trials, after the post-word blank offset, we could not test the ERP difference between TBF and TBR conditions during the study phase. Future studies

U

could employ additional techniques (e.g., fMRI) to investigate the neural activities

JO

triggered by forgetting cues. 5. Conclusions

In this study, we aimed to investigate whether elaborately rehearsed information could be intentionally forgotten. Behavioural results demonstrated that memory performance was inferior for the TBF words than for the TBR words. The ERP results indicated that the TBF words showed more negative FN400 and less positive LPC 30

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activities (or reduced ERP old/new effects) compared to the TBR words, indicating worse memory retention for TBF words. This study demonstrated that the forgetting cues elicited a positive effect on the promotion of forgetting the elaborately rehearsed

O

O

F

information, and the memory representation for TBF words might be inhibited.

PR

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Acknowledgements This work was supported by the Natural Science Foundation of Liaoning province [20180550140] and National Natural Science Foundation of China [grant number 39

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31800953]. Competing interests

Figure legends

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The authors declare no competing interests.

Figure 1. Experimental design and procedure. a) Sequence of events in the study phase. No

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explicit cue followed the word in the TBR condition. The red ‘XXXX’ was used as the forgetting cue. b) Sequence of events in the test phase. Event-related potentials (ERPs)

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were time-locked to word onset.

Figure 2. Behavioural performance across conditions for Experiment 1. a) Hit rates. b)

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Recognition reaction times. Error bars represent standard errors of the mean. ***p < 0.001,

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*p < 0.05. TBR, to-be-remembered; TBF, to-be-forgotten.

Figure 3. Grand averaged (n = 31) ERPs for the four kinds of items (TBR-R, TBF-R, TBFF, and CR) during the test phase. Topographic maps indicates the differences between conditions during the 300–500 and 500–800 ms time windows. TBR-R, subsequently remembered to-be-remembered; TBF-R, subsequently remembered to-beforgotten; TBF-F, subsequently forgotten to-be-forgotten; CR, correctly rejected.

Figure 4. Behavioural performance across conditions for Experiment 2. a) Recognition proportion rates. b) Recognition reaction times. Error bars represent standard errors of the 40

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Highlights

Both TBR and TBF words were instructed to be elaborately rehearsed.

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Superior memory performances was observed for TBR words than for TBF words.

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TBR words evoked less negative FN400 and more positive LPC components than TBF

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Enhanced FN400 and LPC old/new effects were observed for TBR versus TBF items.

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Elaborately rehearsed information could be actively inhibited.

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