Incidental Auditory Learning and Memory-Guided Attention: Examining the ☆ Role of Attention at the Behavioural and Neural Level Using EEG

Neuropsychologia 147 (2020) 107586

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Neuropsychologia

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Incidental auditory learning and memory-guided attention: Examining the ☆ role of attention at the behavioural and neural level using EEG

Manda Fischer a,b,*, Morris Moscovitch a,b, Claude Alain a,b a Rotman Research Institute, Baycrest Hospital, Toronto, Canada b University of Toronto, Department of Psychology, Toronto, Canada

ARTICLE INFO ABSTRACT

Keywords: The current study addressed the relation between awareness, attention, and memory, by examining whether Auditory merely presenting a tone and audio-clip, without deliberately associating one with other, was sufficient to bias Attention attention to a given side. Participants were exposed to 80 different audio-clips (half included a lateralized pure Memory tone) and told to classify audio-clips as natural (e.g., waterfall) or manmade (e.g., airplane engine). A surprise Implicit memory test followed, in which participants pressed a button to a lateralized faint tone (target) embedded in EEG each audio-clip. They also indicated if the clip was (i) old/new; (ii) recollected/familiar; and (iii) if the tone was on left/right/not present when they heard the clip at exposure. The results demonstrate good explicit memory for the clip, but not for tone location. Response times were faster for old than for new clips but did not vary ac cording to the target-context associations. Neuro-electric activity revealed an old-new effect at midline-frontal sites and a difference between old clips that were previously associated with the target tone and those that were not. These results are consistent with the attention-dependent learning hypothesis and suggest that asso ciations were formed incidentally at a neural level (silent memory trace or engram), but these associations did not guide attention at a level that influenced behaviour either explicitly or implicitly.

1. Introduction and awareness that mediate memory and attention when a person listens to audio-clips of everyday real-world environments. Experimental Psychology is shifting focus from studying cognitive processes in isolation to considering them as components in a complex, 1.1. Attention as a mediating factor for the effect of implicit long-term interactive system (Moscovitch et al., 2016; Romero and Moscovitch, memory (LTM) on perceptual organization 2015). Making sense of everyday auditory scenes requires hearing the appropriate signal from the incoming sound mixture. Previous research Previous research suggests that attention is the primary mediating suggests that both low-level acoustic-driven and high-level schema- factor that enhances sensory processing when familiarity of stimuli is driven processes are necessary for successful auditory perception (Alain manipulated. Chun and Jiang (1998) were among the first to demon and Bernstein, 2015; Bregman, 1990). Schema-driven scene analysis strate that memory may influence the deployment of attention and involves the use of learned schemas that are stored in memory in order facilitate target localization. This study, and the majority of subsequent to guide perceptual organization of acoustic input. Attention and studies examining contextual cueing, presented participants with memory, two important and tightly related phenomena, play a vital role randomly generated configurations.Each configurationhad a target that in disambiguating complex acoustic signals in everyday listening situ always appeared in the same location. Old invariant conditions were ations (Backer and Alain, 2013; Backer et al., 2015). Most research has those that repeated throughout the entire experiment. Participants were focussed on the effects of attention on memory; few studies have not told to memorize the spatial arrangement of the distractors or the investigated the converse, that memory may guide attention. The pro target location. Their response times, however, were faster when the posed study seeks to examine the relation among learning, attention, target was embedded in old invariant configurations compared to new

☆ This research was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grants to CA [RGPIN-2016-05523] and to MM [A8347]. * Corresponding author. Rotman Research Institute, Psychology, University of Toronto, Toronto, Canada. E-mail address: [email protected] (M. Fischer). https://doi.org/10.1016/j.neuropsychologia.2020.107586 Received 13 January 2020; Received in revised form 16 July 2020; Accepted 16 August 2020 Available online 17 August 2020 0028-3932/© 2020 Elsevier Ltd. All rights reserved. M. Fischer et al. Neuropsychologia 147 (2020) 107586 variant conditions. A recognition test at the end of the testing session examined is the extent to which incidental associations between context was used to determine the nature of the participants’ knowledge of the and target can also facilitate memory-guided attention. The repeated configurations. The results indicated that explicit memory for attention-dependent learning hypothesis posits that expression of the configurations themselves were at chance level (52%). Based on learning, but not learning of associations themselves, in terms of a these results, the authors concluded that implicit processes facilitated behavioural benefit,depend on task relevance and attention. Therefore, the encoding of context which, in turn, influenced and constrained in order to confirm whether incidental learning and implicit processes expectation and visual search behaviour (e.g., Chun and Jiang, 1998; can guide attention at the behavioural level, a paradigm that tests for the Chun and Jiang, 2005). Interestingly, however, three out of 14 partici incidental learning of the associations themselves is needed. pants (Experiment 1) and seven out of 18 participants (Experiment 5) reported being aware that certain configurations were repeated. Even 1.2. Current study though awareness of repetition was not associated with explicit recall of the configurations, one cannot rule out the possibility that memory The current experiment aims to address these limitations, by exam representations for configurations might have been contaminated by ining the role of attention at encoding on memory-guided attention at explicit processes. retrieval. Here, we investigated whether the effect of memory-guided Zimmermann et al. (2017) examined the effect of memory-guided attention holds in natural listening situations in which incidental asso attention in audition. They showed that deliberately forming associa ciations are formed through implicit learning (exposure). By not having tions between audio-clips and tones enables memory to bias attention to participants deliberately associate the target and the clip at encoding, auditory stimuli. Participants were instructed to pay attention to, and we provided the conditions at learning necessary to implicate implicit form an association between, an audio-clip and the spatial location of an processes. Additionally, we included a forced-choice question about the embedded lateralized pure tone target. The results of a subsequent test association between clip and target in order to test objectively for im on participants’ memory for the learned associations exhibited facilita plicit learning and awareness of the associations formed (Shanks, 2005). tion of target localization. This benefitwas observed despite the fact that The paradigm used by Chun and Jiang (1998) has an unaware participants were unable to consciously report the association between element with repeated meaningless geometric configurations. Other audio-clip and spatial location. The authors interpreted these findingsas studies by Patai et al. (2012) use meaningful stimuli but rely on explicit evidence of a separate implicit system at play, independent from any knowledge of the target location in relation to the context (e.g., target to explicit knowledge. the left of the beach umbrella). Our study combines elements of both of It is unclear, however, whether incidental learning of the association these paradigms to address implicit processing within real-world between context and target and independent implicit processes are truly contexts. implicated in these studies. A number of criteria have been established The validity of this effect was tested behaviourally, and the neural to assess awareness (Reingold and Merikle, 1990; Shanks and St John, correlates underlying this memory-retrieval process were examined 1994). Chun and Jiang (1998) violated the information criterion criteria using electroencephalogram (EEG). Specifically, we aimed (1) to by not asking participants to report the nature of their memory for the examine further the link between auditory memory and attention, by target-context association. Although participants’ memory for the testing whether incidental associations between tone and audio-clip context may be implicit, it is unknown whether or not they can explicitly facilitated localization of a lateralized pure tone (i.e., target); and (2) express context-to-target associations. This information regarding the to use EEG to index neural (implicit) processes underlying this effect. association is presumably what guides attention to afford a behavioural Rugg et al. (1998) used event-related potentials (ERPs) to reveal benefit. Therefore, in order to truly test for implicit learning, the test separate neural patterns of memory-related activity. Contrasts between used must measure the same stored knowledge that is influencing old recognized and old unrecognized words and new and old unrecog behaviour (Dulany, 1961; Shanks and St John, 1994). nized words in a recognition task over parietal areas of the scalp Zimmermann et al. (2017) trained participants to explicitly pair the revealed the neural dissociation between implicit and explicit memory. context with the target location. At test, however, they used “absence of Furthermore, to address the issue of simply studying the difference be explicit recall” of these associations as a metric for implicit memory. tween recognized and unrecognized items in the standard recognition This is problematic, as previous studies have demonstrated above paradigms, Paller et al. (1998) conducted a study to manipulate the chance performance on implicit tasks may still occur without a clear amount of priming, independent of influences on recollection. This dissociation between recognition and priming. Statistical anomalies and paradigm allowed for the identification of a unique ERP correlate over noise introduced into a model for explicit learning can yield these occipital sites, indexing implicit memory. Although we used different dissociative results (Ostergaard, 1992; Plaut, 1995; Poldrack et al., procedures and materials, in the current study, we predicted that ERPs 1999; Shanks, 2005). Therefore, these tests do not rule out contamina would show a difference during the sustained potential over parietal and tion from explicit memory processes. auditory temporal sites between clips that had been associated with the The fact that participants were instructed to do the same task both at target compared to those that were not, indexing the implicit encoding learning and at test may be additionally problematic. Using different of audio-clip-to-target associations. Evidence of priming in the auditory tasks at learning and at test can minimize contamination of implicit cortex would complement the findingsof Paller et al. (1998), who found memory by explicit memory systems and allow for differential “transfer- an electrophysiological measure of priming over occipital sites for visual appropriate processing” across conditions (Paller et al., 1998; Schacter stimuli. et al., 2007). If attention at learning is not manipulated, contamination The results of the current study revealed neural differences indica between explicit and implicit memory systems cannot be ruled out tive of the formation of a neural trace/engram of the learned associa (Wolters and Prinsen, 1997). Therefore, whether implicit learning can tions between tone presence and audio clip (i.e., auditory scene), but no indeed facilitate memory-guided attention to auditory objects remains differences at the level of behaviour (i.e., reaction times for localizing an open question. the pure tone). For the remainder of the paper, we will refer to effects Together, the literature on memory-guided attention suggests that observed with EEG as reflective of a neural trace/engram and behav when attention is drawn to either (i) the target but not to the context (e. ioural effects as reflectiveof implicit memory. The dissociation between g., Chun and Jiang, 1998; Chun and Jiang, 2005) or (ii) the association a neural memory trace and an implicit memory (the behavioural between scene (context) and tone (target) (Zimmermann et al., 2017), consequence) are discussed in detail in the Discussion section. memory-guided attention is facilitated. However, what has not been

2 M. Fischer et al. Neuropsychologia 147 (2020) 107586

2. Methods

2.1. Participants

Twenty-six healthy young adults participated in the experiment. Data from one participant was removed due to issues with task compliance. The remaining 25 participants (M = 26.1 years; SD = 4.3; 10F) had normal hearing, as assessed using pure tone audiometry, and had no history of psychiatric, neurological, or other major illnesses. Effect sizes pertaining to the main effect of memory cue in three ex periments described in Zimmermann et al. (2017) (Cohen’s dz = 1.53, 0.58, and 0.64, respectively) and in one experiment in Zimmermann et al. (2020) (Cohen’s dz = 0.53) were calculated. We then used the most conservative effect size to compute the estimated power of our study for a paired t-test between dependent variables, using G*Power 3.1.9.4 (Faul et al., 2007). The estimated power achieved was 0.84. Participants were recruited from the Rotman Research Institute participant database and received monetary compensation for their participation. None of the participants in the current study took part in previous experiments of a similar nature. The study is certified for ethical compliance by the Research Ethics Board at Baycrest and all participants provided written consent.

2.2. Stimuli Fig. 1. Paradigm overview. a) Experiment overview, comprising of both exposure and test phases. The exposure phase had participants form incidental A total of 108 everyday audio-clips, selected from "http://www. associations between the sound-clip and target location. The test phase exam freesounds.org/," were included in the experiment. An initial pilot test ined the memory of the clip and its effect on target localization. b) Overview of confirmed that each clip in the set was nameable and that there was a single trial at test phase. Note: Cue audio-clip and probe audio-clip at test considerable consistency among participants. Each clip could be given a represent the firstand second repetition of the audio-clip, separated by an ISI of semantic label (e.g., coughing), which increased the likelihood of an 1000 ms. Only the probe audio-clip contained an embedded pure tone target, association between the clip and the tone to be formed and stored in 2000 ms after probe audio-clip onset. The memory-cue condition had a tone long-term memory (Cohen et al., 2011; Snyder and Gregg, 2011). Clips embedded in the left or right ear, at exposure. At test, the tone (i.e., target) was were cut from their original length to a duration of 2500 ms with a 100 then presented at the same location. Neutral-cue and new clips did not have a tone embedded in them at exposure. At test, neutral-cue and new clips had a ms rise and fall time. In addition, all clips were down-sampled to a tone (i.e., target) embedded in the left or right ear (randomized and counter standard sampling rate of 44100 Hz. All stimuli were presented through balanced). Therefore, all conditions had a target embedded in them at test insert earphones (EARTONE 3a), at a listening volume of 65 decibel (dB) during the probe audio-clip. sound pressure level (SPL) on average across stimulus duration, with brief peak amplitudes of 80 dB SPL. ear) pure tone stimulus. Prior to the study, we ensured that the pure tone Eighty clips were used during the exposure phases, in which 20 were was clearly audible (suprathreshold 80 dBA SPL), allowing implicit paired with a left ear auditory target and 20 with a right ear auditory incidental learning, via mere exposure, to proceed. During the presen target. These clips (referred to as old items) were also presented at the tation of the sound clip, participants were instructed to fixate on the surprise memory-test phase. In addition to the “old” clips, twenty-four cross at the center of the black screen. For each trial, participants indi “new” clips were introduced at the memory-test phase. These clips did cated whether the audio-clip depicted a natural (nature) scene (e.g., not have any prior associations between them and the target location. waterfall) or a manmade object (e.g., airplane engine). In line with the A pure tone target (500 Hz, 500 ms in duration, 50 ms rise/fall time) incidental nature of encoding, we made no reference to the embedded was embedded in 50% of the clips at exposure (80 dBA SPL) and in all tone or to any memory test. To respond, participants used the “left” and clips at test (55 dBA SPL). In all cases, the pure tone was embedded 2s “right” arrow keys on a computer keyboard. Key-response was pseudo- after clip onset. The lateralization of the tone was counterbalanced and randomized across participants, in that half of the participants had randomized for each participant. The sound level at which the pure tone “left” and “right” keys corresponding to natural and manmade, respec target was played within the audio-clip was constant across participants. tively, and the other half had “left” and “right” keys corresponding to The screen was black with a white fixationcross at the center during the manmade and natural, respectively. Clip order was randomized across presentation of auditory stimuli. Acoustic stimuli and visual cues were exposure phases and participants. In addition, left-lateralized, right- presented, using Presentation software (version 13, Neurobehavioral lateralized, and neutral-cue clip pairings with clip were randomized Systems, Albany, CA). Sound levels were measured, using a Larson Davis across participants. This ensured that any effects uncovered would not System 824 and a 2CC coupler. be attributable to key-response, order-of-clips, or specific pairing be tween clip and spatial location. 2.3. Procedure

Participants were first fittedwith an electrode cap and prepared for 2.5. Test phase (retrieval) EEG recording. Then, they were presented with the exposure and the test phases (see Fig. 1). After the exposure phase, participants were given a surprise memory test (retrieval) on the learned associations. In each trial, participants 2.4. Exposure phase (encoding) were presented with a cue, followed by a brief delay and a probe audio- clip that included a faint lateralized target tone (i.e., 55 dBA SPL). An In the exposure phase, participants were presented with four blocks initial pilot test was conducted by Zimmermann (2018), demonstrating of 80 audio-clips; half of them comprised of a lateralized (left or right that a single probe was not sufficient to allow participants to activate

3 M. Fischer et al. Neuropsychologia 147 (2020) 107586 auditory memory for the target location. We conducted a pilot study, filtered with 0.1 Hz high-pass filter (forward, 6dB/octave) and 20 Hz with a sample of six participants, in which participants detected the low-pass filter (zero phase, 24 dB/octave). target. The duration and intensity of the target tone was chosen based on For each participant, a set of ocular movements was identifiedfrom their performance, such that the target was not entirely masked by the the continuous EEG recording and then used to generate spatial com clip (approximately 80–90% correct localization), thereby remaining ponents that best accounted for eye movements. The spatial topogra audible. This was done to ensure that all participants engaged in phies were then subtracted from the continuous EEG to correct for effortful listening (Alain et al., 2018; Pichora-Fuller et al., 2017). lateral and vertical eye movements as well as for eye-blinks. After cor The test was comprised of old and new audio-clips. The old audio- recting for eye movements, all experimental files for each participant clips were divided into memory and neutral-cue clips. The memory- were then scanned for artifacts; epochs including deflectionsexceeding cue clips included a lateralized tone during the exposure phase. The 120 μV were marked and excluded from the analysis. The remaining neutral-cue clips did not include a lateralized tone during exposure. In epochs were averaged according to electrode position and experimental addition, we included catch trials in which the pure tone target was conditions. Each average was baseline-corrected with respect to a 200 presented in the opposite ear to the one used during the exposure phase. ms pre-stimulus baseline interval. Approximately 2–15% of trials were The ratio between memory-cue and catch trials was 80:20. During the rejected for each participant. presentation of the sound clips, participants were instructed to fixateon The data were parsed into two sets of epochs: Cue audio-clip and the cross at the center of the black screen. probe audio-clip. The cue audio-clip epochs started 200 ms before clip Participants were required to indicate 1) if, at test, the tone was onset (0 ms) and ended 2000 ms after the cue onset. We also used the presented on the left or on the right (localize faint pure tone as quickly as same epoch length and filter settings to examine neuroelectric activity possible with key press); 2) if the audio-clip was old or new; 3) when old, preceding the target tone (i.e., probe audio-clip). if they recollected the audio-clip or if it was merely familiar from exposure; and 4) if, at exposure, the tone was either on the left, right, or 3. Statistical analyses not present. Participants used the “left” and “right” arrow keys for questions 1–3 and “left”, “right”, and “down” arrow keys for question 4. Catch trials were not analyzed, as there were too few correctly- If participants responded “New” to question 2, the experiment pro localized trials (at most 4 left and 4 right per participant) to calculate ceeded to the next trial and did not present questions 3 and 4. Key a reliable average reaction time for this condition. Therefore, assessing response was pseudo-randomized across participants for questions 2 and the potential cost/benefit of the memory-guided attention effect, by 3, in which half of the participants had “left” and “right” keys corre comparing old memory-cue clips to old catch trials, was not possible. sponding to old and new, as well as recollect and familiar, respectively, and the other half of participants had “left” and “right” keys corre 3.1. Behavioural sponding to new and old, as well as familiar and recollect, respectively. Clip order was randomized across participants. This procedure ensured Reaction time (RT) and percent accuracy were measured at test that any effects uncovered would not be attributable to key-response phase. RT and percent accuracy for natural and manmade responses at and order-of-clips, respectively. exposure were recorded and documented for potential future analyses. Question 3 (Recollect/Familiar?), common to traditional memory paradigms, was included in order to disentangle processes underlying 3.1.1. Old-new effect recollection of the clip. Recollection was defined as a sound that par In order to assess the contextual component of memory-guided ticipants “can remember, from [their] own perspective [...] because attention, old clips (memory-cue and neutral-cue) were compared to [they] can remember additional details associated with it.” Familiar was new clips, using a paired two-sample t-test. The analysis used RT as the defined as a sound that participants “can recognize […] but can’t dependent variable and clip type (new or old) as the independent vari remember any additional details associated with it. Nonetheless, [they] able. It was expected that responses on trials that contain old clips would have the strong impression, or are even sure, that it occurred earlier in be faster than those that contain new ones, as the former should have the experiment.” already had an existing long-term representation of the clip.

2.6. EEG recording and analysis 3.1.2. Memory-guided attention effect To assess the memory-guided attention component of this effect, old The EEG was recorded continuously during each exposure phase and memory-cue clips were compared to old neutral-cue clips, using a paired during the memory-guided attention test phase, using a 76-channel two-sample t-test. The analysis used RT as the dependent variable and acquisition system (BioSemi Active Two, Amsterdam, The clip type (old memory-cue or old neutral-cue) as the independent vari Netherlands). Sixty-six EEG electrodes were positioned on the scalp, able. It was predicted that there would be a benefit in RT in trials that using a BioSemi headcap, according to the standard 10/20 system, with contain old memory-cue clips compared to those that contain old a Common Mode Sense (CMS) active electrode and Driven Right Leg neutral-cue clips, as old memory-cue clips would have already formed (DRL) ground electrode. Ten additional electrodes were placed below associations between clip and spatial location that may aid in focussing the hairline (two symmetrical electrodes on the mastoid, pre-auricular attention. Conversely, old neutral-cue clips were not expected to have an points, outer canthus of each eye, inferior orbit of each eye, and two association between clip and spatial location. Therefore, it was pre facial electrodes) to monitor eye movements, as well as to cover the dicted that target localization for these types of clips would be slower whole scalp evenly. After low-pass filtering at 100 Hz, the EEG was than for old memory-cue clips. sampled at rate of 512 Hz, digitized, and stored continuously for offline analysis using the Brain Electrical Source Analysis software (BESA, 3.1.3. Recollect and familiar effect version 6.1; Megis GmbH, Grafelfing,¨ Germany). To investigate the potential memory system that underlies explicit Data pertaining to five participants were not used because of retrieval of the sound-clip, we examined whether sound-clips that were excessive eye movements and/or muscle artifacts. As a result, 20 par correctly categorized as old were recollected or familiar. Although ticipants were included in the EEG analysis. The EEG data were first recognition of the sound-clip itself was not the main focus of the paper, visually inspected to identify segments contaminated by defective we nevertheless wanted to better understand how explicit processing of electrode(s). No more than ten electrodes were interpolated, using the clips might have affected incidental encoding and processing of the values from the surrounding electrodes. The EEG was then re-referenced associations between sound-clip and target tone. It is possible that RT for to the average of all electrodes. The continuous EEG was digitally localizing the pure tone at test differs for recollected and for familiar

4 M. Fischer et al. Neuropsychologia 147 (2020) 107586 sound-clips. Despite the fact that the memory-guided attention effect .38, d = 0.18, BF10 = 0.30, respectively, suggesting that they could was not observed behaviourally, we compared RT for recollected and explicitly report neither the tone’s location (memory-cue) nor its pres familiar clips to first see if there were any marked differences between ence or absence (neutral-cue). All comparisons were Bonferroni the two dependent measures. corrected. Furthermore, clips that were deemed “missed” were those that were old but were judged by the participant as new (i.e., implicit memory of 4.1.2. Old-new effect the sound-clip). We had hoped to analyze missed trials, but the number The average RT for localizing the pure tone at test for correctly of trials for this condition was too low due to above chance accuracy at categorized old clips (M = 690.82 ms, SE = 34.07) was compared to the correctly classifying the sound-clips as old or new. average RT for correctly categorized new clips (M = 734.62 ms, SE = 42.40). The contrast yielded a significant difference between the two 3.1.4. ERP statistical analyses conditions, t(24) = 2.56, p = .009, d = 0.52, suggesting that memory for For statistical analyses, the ERP waveforms were exported into BESA the clip facilitates target localization (Fig. 3 left panel). Statistics 2.0. BESA Statistics 2.0 software automatically identifies clusters in time and space, using a series of t-tests that compared the ERP 4.1.3. Memory-guided attention effect amplitude between experimental conditions at every time point. This Contrasts between average RT in localizing the pure tone at test for preliminary step identified clusters both in time (adjacent time points) correctly categorized memory- and neutral-cue conditions did not yield and space (adjacent electrodes) where the ERPs differed between the a significant difference, t(24) = 1.14, p = .26, d = 0.23, BF10 = .375 conditions. The channel diameter was set at 4 cm which led to roughly (Fig. 3 right panel). four neighbours per channel. A cluster alpha of .05 for cluster building was used. A Monte-Carlo resampling technique (Maris and Oostenveld, 4.1.4. Recollect and familiar effect 2007) was then used to identify those clusters that had higher values Audio-clips that were categorized as old were further categorized as than 95% (one-sided t-test) of all clusters derived by random permuta either recollected (MPercent Old = 55.38%, SE = 3.81) or familiar (MPercent tion of the data. The number of permutations was set at 1000. Old = 44.62%, SE = 3.81). A two-way repeated measures analysis of Cluster-based statistics were performed on two different time win variance (ANOVA) was conducted to compare RTs for memory-cue and dows: cue audio-clip and probe audio-clip. For old and new audio-clips, neutral-cue conditions in terms of the recognition memory involved. The = = 2 = it was expected that ERPs would show a difference during cue audio- analysis showed a significantinteraction, F(1, 24) 5.62, p .03, ηp clip, indicating that information related to the clip was being retrieved .19 (Fig. 4). Post-hoc Bonferroni corrected t-tests revealed no significant from LTM and maintained in working memory (Awh and Jonides, 2001; differences between the pairwise comparisons, p > .05. Bae and Luck, 2017; Zimmermann et al., 2020). For memory-cue and As there were no differences in accuracy, and the interaction neutral-cue clips, it was expected that ERPs would differ in their sus observed in RT was not predicted, we have no ready interpretation for tained potential, indicating that a neural trace reflecting the formation these results. One possibility is that in the memory condition, recollec of associations between audio-clip and target. tion brings to mind a tone, but not its location, thereby distracting the participant at test and slowing down responses compared to the famil 4. Results and comment iarity condition when no contextual cue (tone) is recalled. Because no tone was presented at exposure in the neutral-cue condition, recollec 1 4.1. Behavioural results tion, compared to familiarity, led to more rapid processing of neutral- cue clips. Overall memory accuracy for old and new audio-clips (question 2: Old versus New) and the sound-tone association (question 4: Left, Right, 4.1.5. Electrophysiological results at exposure phase (encoding) = = None) were assessed. The results reveal that old (M 77.3%, SE 2.40) In order to rule out the possibility of attentional capture/distraction = = and new (M 78.2%, SE 2.30) clips were correctly categorized as old by the tone at exposure, we examined group mean ERP at exposure. = < = and new above chance level (50%), t(24) 11.13, p .001, d 2.22 and Fig. 5 pertains to group averaged ERPs for trials that contained the left or = < = t(24) 12.04, p .001, d 2.41, respectively (Fig. 2 left panel). There right tone (memory-cue) and for trials that did not contain a tone was no significantdifference between memory accuracy for recollected (neutral-cue), time-locked and baseline corrected, using 100 ms prior to = = = = clips (M 88.57% SE 0.03) and for familiar clips (M 89.22%, SE the onset of the tone. Both left and right ear tones embedded in the audio = = = 0.04), t(24) 0.157, p .88, d 0.03. Hits minus false alarms for clip clip generated an acoustic change complex (ACC), which was expected. = = accuracy (M 55.5%, SE 2.95) was also significantlyabove chance, t There was no evidence of a P3a. The presence of ACC and lack of P3a = < = (24) 18.84, p .0001, d 3.77, suggesting that participants were suggest that the tones were clearly perceptible, but that they did not capable of distinguishing between old and new items. capture nor yield a major reorienting of attention.

4.1.1. Sound-tone association 4.1.6. Electrophysiological results at test phase (retrieval) Accuracy for reporting whether, for memory-cue and neutral-cue Fig. 6 shows group mean ERPs elicited by the cue and probe audio- clips, the target tone was on the left, right, or not present during expo clips. The onset of both was associated with large transient evoked sure, was compared to chance accuracy (33%), using a one-sample t-test. responses. The results revealed that participants performed at chance level when The contrast assessing whether ERPs differed between old and new = asked to report the tone’s location relative to the particular clip, t(24) and memory-cue and neutral-cue clips was performed from 0 to 2000 ms = = = + 1.62, p .12, d 0.35, BF10 2.04e 15 (Fig. 2 right panel). Using a relative to stimulus onset (i.e., cue or probe onset). We did not assess one-sample t-test, sound-tone accuracy was analyzed separately for whether ERPs differed between correctly recollected and familiar clips memory-cue clips (left/right vs. no tone) and for neutral-cue clips (no due to an insufficient number of trials. tone vs. left/right). Participants still performed at chance level (50%), t = = = = = = (24) 0.04, p .97, d 0.008, BF10 0.21 and t(24) 0.89, p 4.1.7. Cue audio-clip (0 ms–2000 ms) Generally, the cue audio-clips generated transient onset responses that were largest at midline central electrodes, and which were followed by a sustained potential over the left central, temporal and temporal- 1 All Cohen’s d calculations were computed using the following formula: d = t parietal sites. √N

5 M. Fischer et al. Neuropsychologia 147 (2020) 107586

Fig. 2. Group mean accuracy at test phase. Left panel: Memory accuracy for old and new clips (Q2: Old or New?). Right panel: Memory accuracy for sound-tone association for memory-cue clips. (Q4: At exposure, was target on left, right or no target?). Chance level of 33% was determined based on the three choices pro vided in question 4 (left, right, none). Error bars represent standard error of the mean.

Fig. 3. Reaction times (RT) for localizing the faint pure tone at test. Q1: At test, localize tone on the left or right. Left panel: RT for localizing the pure tone at test for correctly categorized old and new clips. Old clips were comprised of both memory-cue and neutral-cue clips. Right panel: Average tone-localization RT for correctly “categorized as old” memory-cue and neutral-cue clips. Error bars represent standard error of the mean.

Fig. 4. Interaction plot depicting RTs for old clips in terms of the recognition type. Q3: At test, is the audio-clip recollected or familiar? Group mean RT for localizing the faint pure tone at test for correctly remembered old recollected and familiar clips. Error bars represent standard error of the mean. Fig. 6. Butterfly plot of group mean ERPs. Grey boxes depict the sub-events. The grey lines show ERPs from all scalp electrodes. The black line shows ERPs at the midline fronto-central electrode (FCz). For illustration purposes, the data were filtered (high-pass filter = 0.4 Hz and low-pass filter = 10 Hz). The sustained potential was filtered out to emphasize the transient onset and offset responses of each sub-event.

Old vs. New. In this analysis, we examined whether there were neural indices underlying the behavioural difference in new and old clips. ERP averages for old clips included both memory-cue and neutral- cue clips. Cluster permutations yielded fivesignificant clusters (Table 1, Fig. 7). The firstcluster was associated with enhanced positivity for old over new clips over parietal areas of the scalp at 777–1072 ms, which Fig. 5. Group mean event-related potentials (ERPs) at exposure. ACC = reversed polarity at frontal sites (Table 1, Cluster 3). The second cluster = acoustic change complex. Fz midline frontal electrode. followed the first one in time and revealed enhanced negativity at 1307–1998 ms for old over new clips over lateral frontal scalp area. The third cluster overlapped with the first cluster in time and showed

6 M. Fischer et al. Neuropsychologia 147 (2020) 107586

Fig. 7. Left panel: Group mean ERPs for the cue audio-clip: Old vs. New. The grey boxes depict significant time windows. Dark grey represents overlapping time windows. Right panel: For this and subsequent figures,the iso-contour maps show the group mean amplitude over a predefinedwindow around the peak amplitude. The time window for Cluster 1 and 2 were 900–1000 ms and 1300–1400 ms, respectively. P1 = left parietal electrode; FC4 = right fronto-central electrode.

Table 1 Cue audio-clip: Summary of the channel level cluster-based permutation statistics for Old vs. New audio-clips.

Contrast Cluster Latency (ms) P value Electrodes

Old vs. New 1 777–1072 p < .0001 FC3, FC1, C1, C3, C5, CP5, CP3, CP1, P1, P3, PO3, POz, Pz, CPz, FCz, Cz, C2, TP8, CP6, CP4, CP2, P2, P4 2 1307–1998 p = .001 F4, F6, F8, FC6, FC4, FC2, FCz, C4, CP4, CP2, P2 3 885–1004 p = .02 FP1, FPz, FP2, AF8, FT10, F10, LO2, IO2 4 662–742 p = .002 CP5, CP3, CP1, P1, P3, P7, PO3, Oz, POz, Pz, P2, PO4, O2 5 506–666 p = .02 FC1, C1, C3, CP3, CP1, P1, Iz, Oz, POz, P2, PO8, O2 modulations over the frontal scalp area. The fourth and fifth cluster than for old ones (Table 3 and Fig. 9). overlapped one another, preceded all other clusters in time and showed Memory-cue vs. Neutral-cue. Next, we compared memory- and modulations in the central-parietal and parietal areas of the scalp. neutral-cue clips. The ERP analyses yielded two significantclusters. The Correlations between memory accuracy for old clips and the absolute first significant cluster was located over frontal regions, with memory- difference in ERP amplitude between old and new clips were computed cue clips eliciting greater sustained negativity than neutral-cue clips for each cluster latency. These correlations were not significant,p > .05. (Table 4 and Fig. 10). The second cluster followed the first cluster in Memory-cue vs. Neutral-cue. Cluster permutation yielded one time and occurred over right parietal areas of the scalp, with greater significantcluster over frontal and fronto-central areas, with neutral-cue sustained negativity for neutral-cue clips than for memory-cue clips due clips eliciting greater sustained negativity than memory-cue clips to a reversal in polarity from anterior to posterior sites (Table 4 and (Table 2, Fig. 8). We also tested whether ERP activity would differ when Fig. 10). audio-clips were paired with a left or a right-lateralized auditory target. No significant difference was observed (p > .05). 5. Discussion

4.1.8. Probe audio-clip (0 ms–2000 ms) The current study further investigated the role of attention at Old vs. New. The ERP analyses yielded two significantclusters. The encoding on memory-guided attention at retrieval. We tested whether first significant cluster was located over right central, temporal, and mere exposure can facilitate memory-guided attention to real-world parietal areas of the scalp, with old clips eliciting greater sustained sounds. The results show that when conditions at learning are condu negativity than new clips, due to a polarity reversal from anterior to cive to the incidental encoding of associations between sound-clip posterior sites (Table 3 and Fig. 9). The second cluster overlapped with (context) and tone (target), explicit memory for the clip is good, but the first cluster in time and occurred over left and midline frontal and memory for the tone’s presence and location is at chance. Target central areas of the scalp, with greater sustained negativity for new clips localization was also faster for old clips with or without an embedded

Table 2 Cue audio-clip: Summary of the channel level cluster-based permutation statistics for Memory-cue vs. Neutral-cue audio-clips.

Contrast Cluster Latency (ms) P value Electrodes

Memory-cue vs. Neutral-cue 1 1020–1100 p = .03 AF3, F1, F3, AF4, Fz, F2, FC2, FCz

7 M. Fischer et al. Neuropsychologia 147 (2020) 107586

associated with ‘target present’ and neutral-cue associated with ‘target absent’) was formed. The EEG results pertaining to the difference be tween memory-cue and neutral-cue clips may index the formation of this memory trace, while the behavioural results pertaining to the lack of difference between memory-cue and neutral-cue clips suggest that this learned association was not expressed at the behavioural level. Together, these results support the latent learning and attention-dependent learning hypothesis that learning of the association itself does not require directed attention (Chun and Jiang, 2005), but expression of learning in the form of behavioural enhancement does require attention (Treisman and Gelade, 1980), respectively. Specifically, in relation to memory-guided attention, when the association between context and target is truly incidentally encoded, we do not findevidence for implicit processes playing a role in guiding auditory attention at the level that influences behaviour. In the current study, our memory to attention paradigm can also be construed as auditory priming for non-verbal information. Church and Schacter (1994) found that, for words, if acoustic features, such as speaker voice, intonation, and fundamental frequency are altered, per formance is worsened, or priming effects are completely eliminated. In our paradigm, the tone, when localized at test, can be thought of as a measure of priming of the sound-tone association. Based on Church and Schacter (1994), one might have expected that detection (priming) would be better in the memory condition, with the tone lateralized on the same side at study and test, rather than in the neutral-cue condition because the acoustic features would remain unchanged. This outcome was not evident in behaviour, suggesting either that non-verbal stimuli, the embedded tone, the task itself (localization) or all three are not sufficiently powerful conditions to lead to behavioural priming. As no-one, to our knowledge, has looked at nonverbal auditory priming, it is interesting to consider these findings in light of Church and Schacter (1994), and determine, in future experiments, whether they provide some boundary conditions for obtaining auditory priming. It is impor tant to note, however, that tone-presence vs tone-absence does lead to Fig. 8. Left panel: Group mean ERPs for the cue audio-clip: Memory-cue vs. Neutral-cue. The grey boxes depict significant time windows. Right panel: The neural priming, indicating that the stimuli can leave a neural trace that iso-contour maps show the group mean amplitude for the 1000–1100 ms in is not realized in behaviour. terval. F2 = right frontal electrode. 5.1. Old-new effect target than for new clips, suggesting that memory facilitates processing of the tone by speeding responses to it. These behavioural effects support The fact that old clips elicited shorter response times compared to previous research that report processing efficiency due to decreased new ones suggests that familiarity with the context may speed responses demand on attentional systems over the course of repetition (Schneider by allowing attentional resources to be allocated to processing the and Shiffrin, 1977). Consistent with these findings and as with explicit target. This conclusion is consistent with previous studies that have behavioural tests, neuro-electric activity revealed an old-new effect at shown facilitation of RTs for old relative to new arrangements when midline and frontal sites. engaging in visual (Chun and Jiang, 1998) and tactile (Assumpçao˜ et al., RTs did not vary as a function of the associations between target 2015; Nabeta et al., 2003) search tasks. In our paradigm, endogenous presence and audio-clip. Importantly, neuroelectric activity yielded a control, which was comprised of habits developed over time as a result significant difference between clips that had been associated with the of repeated exposure, may have facilitated use of the context for sub target compared to those that were not associated with it, yet ERPs were sequent target localization. When one encounters the same context in not lateralized. The difference in ERPs between memory-cue and the future, habitual search enables attention to be guided towards neutral-cue clips may reflect the formation of a neural trace/engram of relevant information, while requiring fewer cognitive resources and the association. Research has shown that silent engrams are memory allowing for resources to be used for processing the target (Le-Hoa Vo˜ traces in the brain that do not control behaviour and are a product of and Wolfe, 2015; Thompson and Sabik, 2018; Trick et al., 2004). normal mnemonic processing (for a review see Josselyn and Tonegawa, The behavioural old-new effect is supported by the ERP analyses, 2020). In other words, the memory of the association exists orthogonal which showed a number of significantmodulations at cue audio-clip and to the recovering of the memory (Moscovitch, 2007). The results suggest probe audio-clip. The old-new effect revealed that new stimuli elicited that a trace of the associations, not specificto the tone’s location per se, greater sustained negativity than did old stimuli over midline and but rather to the presence or absence of the tone (i.e. memory-cue frontal sites. This effect was mirrored in lower inferior areas of the scalp as a polarity reversal. This finding is consistent with previous research

Table 3 Probe audio-clip: Summary of the channel level cluster-based permutation statistics for Old vs. New audio-clips.

Contrast Cluster Latency (ms) P value Electrodes

Old vs. New 1 516–1998 p = .0007 AF8, FT8, FC6, C6, T8, TP8, CP6, CP4, P8, P10, PO8, CB2, TP10, FT10, F10, LO2 2 1311–1645 p = .04 F1, F3, FC1, C1, CP3, CP1, Fz, FCz, Cz

8 M. Fischer et al. Neuropsychologia 147 (2020) 107586

Fig. 9. Left panel: Group mean ERPs for the probe audio-clip: Old vs. New. The grey shaded box denotes significant differences between old and new clips. Right panel: The iso-contour maps show the group mean amplitude for cluster 1 and 2, with 1900–2000 ms and 1500–1600 ms intervals, respectively. F1 = left frontal electrode; C6 = right central electrode. that has shown greater positivity for old compared to new items (Mog perceptually grouped and foregrounded is thought to be prioritized for rass et al., 2006). The early modulation may correspond to familiarity attention (Mazza et al., 2005; Nakayama et al., 1989) and contextual for the audio-clip. The left parietal old-new effect has been associated learning (Jiang and Leung, 2005; Pollmann and Manginelli, 2009). with memory processing (Curran, 2000; Donaldson and Rugg, 1998; Jiang and Leung (2005) concluded that learning of context occurs Friedman and Johnson, 2000; Rugg and Curran, 2007; Vilberg et al., independently of attention and that the effect of memory-guided 2006; Vilberg; Rugg, 2007; Wilding, 2000). In addition, the later sus attention is influenced by where attention is directed at exposure. In tained activity may index maintenance of the audio-clip in working the current study, attention was guided towards the clip at exposure, memory, as participants were not instructed to make a response during rather than the target. At test, however, attention was guided towards the cue audio-clip. the target. It is possible that at test, the target may have already been established as the background. This possibility may account for the strong memory for the clip (foreground) and poor memory for the tar 5.2. Memory-guided attention: memory-cue clips vs. neutral-cue clips get’s location at exposure (background). Therefore, the incidental learning of the associations between clip and target and its behavioural The behavioural results revealed that participants’ memory for the manifestation may be particularly sensitive to the degree to which clip was significantly above chance, but their memory for the sound- attention is manipulated at test and learning may consequently strongly tone association was not significantly different from chance. There depend on which auditory object is attended at encoding. was no significant difference in RT to lateralized targets when Taken together, the behavioural results suggest that the effect of comparing old clips that contained a memory-cue to those that did not memory-guided attention in the case of mere exposure is dependent on (neutral-cue). Therefore, memory for the clip facilitated processing of how the attended object is processed in the auditory scene and on the the target; this effect, however, was not specific to target location or conditions at learning that affect the encoding of the sound-tone asso presence. This suggests that when attention is drawn only to the clip ciation. When attention is drawn to the clip and the association between (background), incidental encoding of the sound-tone association is not clip (context) and tone (target) is formed incidentally, we do not see a strong enough to yield a congruency benefit in RT for localizing the behavioural contextual-cueing benefit. This finding highlights the dif target at test. ference between associations that are formed via mere exposure and The absence of a behavioural effect may be due to conditions during those that are formed in a context in which there is conscious effort, but exposure that may have affected encoding of the sound-tone association. no conscious memory of the associations (Zimmermann et al., 2017, Previous research has shown that visual foreground-background seg 2020). mentation is an important aspect of guiding attention (Wolfe, 2003). By contrast, we did find a significant difference in ERP amplitudes Furthermore, Zang et al. (2016) showed that the perceptual segmenta comparing the memory- and neutral-cue conditions, suggesting that tion of foreground and background precedes, and may even mediate, participants differentially processed these two conditions. It was ex contextual learning, and that only objects that are grouped in the fore pected that a difference in the sustained potential between cue ground are learned over repeated exposure. Information that is

Table 4 Probe audio-clip: Summary of the channel level cluster-based permutation statistics for Memory-cue vs. Neutral-cue.

Contrast Cluster Latency (ms) P value Electrodes

Memory-cue vs. Neutral-cue 1 21–201 p = .01 FP1, AF7, F7, FT7, FC5, T7, FPz, FP2, AF8, AF4, AFz, Fz, F2, AF8, AF4, AFz, Fz, F2, F4, F6, FT9, F9, LO1, IO1 2 104–172 p = .04 P1, PO3, O1, Iz, Oz, POz, CP4, CP2, P2, P4, P6, P8, P10, PO8, PO4, O2, CB2

9 M. Fischer et al. Neuropsychologia 147 (2020) 107586

performance. Therefore, it is possible that the modulations we observe may represent neural signature for implicit processing that has yet to be actualized. Further tests are needed to validate this possibility. Significantmodulations over fronto-central sites may be indicative of propagations reflected from a source located in the auditory cortices. Evidence of priming in the auditory cortex complements the findingsof Paller et al. (1998) who found an electrophysiological measure of priming over occipital sites for visual stimuli. Differences in early and late latencies between the two clusters during the cue audio-clip and probe audio-clip may both reflect atten tional influences.Research suggests that sensory areas can be influenced by attention at different times following onset of a stimulus and can occur as early as 100 ms (e.g., Aine et al., 1995). More work is needed in order to investigate the origin of these pattern of results, regarding di rection and latency. Nevertheless, the findings support the notion that there is neural evidence of a memory trace, indexed by the ERP differ ences between memory-cue and neutral-cue conditions. The fact that there are differences in the neural signature between these conditions suggests that there is residue of prior experience. The lack of ERP lateralization suggests that while there may be an indication of retention of an association (a neural trace/engram), the tone might have blended in with the clip as a Gestalt, leading to the lack of independent encoding of spatial information. Memory-cue clips may contain predictive cues that neutral-cue clips do not, but only in the unitized case (clip + tone). The memory effect distinguishing between memory-cue and neutral-cue clips may reflect anticipation of an item that is not specificto its location. At test retrieval, there may be a pattern completion where the cue either activates the entire Gestalt (clip + tone) or that activates the tone alone. The current study cannot distinguish between these two possibilities. However, the possibility of encoding an entire Gestalt representation of “clip + tone” may explain why the in Fig. 10. Left panel: Group mean ERPs for the probe audio-clip: Memory-cue vs. formation was not used for guiding attention, as measured with Neutral. Right panel: The grey shaded box denotes significant differences be behavioural memory-cue vs. neutral-cue contrast. tween memory-cue and neutral-cue clips. The iso-contour maps show the group The discrepancy between a behavioural effect and a brain effect mean amplitude for the 100–200 ms interval. Fz = midline frontal electrode. brings to light the intricate relationship between attention and learning in relation to memory. Our findings are consistent with previous work conditions would reflect neural processes that support the formation of that has shown that learning the association, in and of itself, as demon an incidental association between audio-clip and target. The neural data strated by the neural difference we findbetween memory- and neutral- showed significantmodulations, corresponding to two separate sources cue conditions, does not require directed attention (Chun and Jiang, at cue audio-clip and probe audio-clip. 2005; Tolman, 1948); expression of this learning, in terms of behavioural The difference between memory- and neutral-cue clips indicates that performance enhancement, however, does require attention (Treisman clips that contain a memory-cue show a significantly different neural and Gelade, 1980). signature from clips that do not. The significant cluster at cue is We show that depending on the task, attention at encoding may be consistent with Zimmermann et al. (2020) who found that memory-cue differentially manipulated and that this can lead to very different clips had greater sustained positivity compared to neutral-cue clips. The behavioural outcomes. This finding highlights the importance of task authors argue that this sustained positivity may reflect greater demand choice. We have provided evidence for the notion that the object to or effort attributed to maintaining two locations/alternatives in working which one attends and the degree to which the associations are made memory for neutral-cue clips compared to memory-cue clips that may explicit at encoding strongly affect the nature of the association at afford the maintenance of a single representation. Furthermore, greater retrieval and how this association may be used for future processing. ERP amplitude for neutral-cue clips than for memory-cue ones may When task conditions are controlled, such that the context-to-target reflectthe fact that neutral-cue clips elicited more prediction violations association is learned incidentally, and contamination from explicit compared to memory-cue clips. Indeed, neutral-cue clips are less infor memory processes minimized, we findthat (i) memory-cue and neutral- mative of the target’s location compared to memory-cue clips. Without cue conditions are neurally distinguishable and form a memory trace, any a priori expectations regarding the spatial location of the tone, but that (ii) these traces require directed attention at encoding in order participants may divide their attention equally between the left and to retrieve them and form an implicit or explicit memory that guides right auditory fields. Consistent with this hypothesis are studies that auditory attention at the level that influences behaviour. have shown that activity related to the attention controlling networks is modulated by the predictability of a certain stimulus event to occur, in 6. Concluding remarks which predictable events have been shown to elicit lower activity than do less predictable ones (Doricchi et al., 2010; Shulman, Astafiev, In sum, the current study contributes to our understanding of the McAvoy, d’Avossa and Corbetta, 2007). nature of implicit and explicit memory processes that guide attention. In The first significant cluster at the probe audio-clip located over the context of memory-guided attention literature, it has been shown frontal areas of the scalp may be consistent with the model proposed by that when a direct association is made at encoding (explicit) between Schacter and his collaborators (Schacter et al., 2007). They found that context and target (Patai et al., 2012; Zimmermann et al., 2017), one activation of frontal cortex is implicated in behavioural implicit memory observes a behavioural effect. The results from the current study add to these findings and help to elucidate the role that attention at encoding

10 M. Fischer et al. Neuropsychologia 147 (2020) 107586 plays in the effect of memory-guided attention. We demonstrate that in Chun, M., Jiang, Y., 2005. Implicit learning of ignored visual context. Psychon. Bull. Rev. – the absence of the formation of an explicit association between target 12 (1), 100 106. https://doi.org/10.3758/BF03196353. Church, B.A., Schacter, D.L., 1994. Perceptual specificity of auditory priming: implicit and clip at encoding (incidental encoding), no effect is observed memory for voice intonation and fundamental frequency. J. Exp. Psychol. Learn. behaviourally, though we do see evidence for a neural trace effect re Mem. Cognit. 20 (3), 521–533. flectedin the neural signature. Therefore, learning conditions that lead Cohen, M.A., Evans, K.K., Horowitz, T.S., Wolfe, J.M., 2011. Auditory and visual memory in musicians and non-musicians. Psychon. Bull. Rev. 18, 586–591. https://doi.org/ to explicit knowledge of the context and implicit knowledge of the 10.3758/s13423-011-0074-0. sound-tone association are not sufficient to guide attention at the Curran, T., 2000. Brain potentials of recollection and familiarity. Mem. Cognit. 28, behavioural level. We acknowledge, however, that some other tests of 923–938. https://doi.org/10.3758/BF03209340. Donaldson, D.I., Rugg, M.D., 1998. Recognition memory for new associations: attention may be more effective in eliciting behavioural evidence asso electrophysiological evidence for the role of recollection. Neuropsychologia 36, ciated with the neural priming we found. As well, some behaviour may 377–395. https://doi.org/10.1016/S0028-3932(97)00143-7. have been influencedby the formed associations but may not have been Doricchi, F., Macci, E., Silvetti, M., Macaluso, E., 2010. Neural correlates of the spatial and expectancy components of endogenous and stimulus-driven orienting of detected by our measures. attention in the Posner task. Cerebr. Cortex 20, 1574–1585. https://doi.org/ Memory-guided auditory attention is a largely unexplored area. 10.1093/cercor/bhp215. Further elucidating the link between memory and attention will help us Dulany, D.E., 1961. Hypotheses and habits in verbal ‘operant conditioning’. J. Abnorm. – better understand memory as a dynamic system (Moscovitch, 1992; Soc. Psychol. 63, 251 263. Faul, F., Erdfelder, E., Lang, A.-G., Buchner, A., 2007. G*Power 3: a flexible statistical Moscovitch et al., 2016; Schacter et al., 2004) that can benefitfrom, and power analysis program for the social, behavioral, and biomedical sciences. Behav. contribute to, attentional processes. This study, also, contributes to the Res. Methods 39, 175–191. fieldof auditory perception, by further definingthe internal mechanism Friedman, D., Johnson, R., 2000. Event-related potential (ERP) studies of memory encoding and retrieval: a selective review. Microsc. Res. Tech. 51, 6–28. https://doi. underlying schema-based scene analysis. The ecological validity of the org/10.1002/(ISSN)1097-0029. proposed paradigm will enable us to adapt it to the world outside the Jiang, Y., Leung, A.W., 2005. Implicit learning of ignored visual context. Psychon. Bull. – laboratory, and aid people who have memory or hearing impairments, Rev. 12, 100 106. https://doi.org/10.3758/BF03196353. Josselyn, S.A., Tonegawa, S., 2020. Memory engrams: recalling the past and imagining such as older adults and those with memory disorders. the future. Science 367 (6473), eaaw4325. https://doi.org/10.1126/science. aaw4325. ̃ CRediT authorship contribution statement Le-Hoa Vo, M., Wolfe, J., 2015. The role of memory for visual search in scenes. Ann. N. Y. Acad. Sci. 1339 (1), 72–81, 10.111/nyas.12667. Maris, E., Oostenveld, R., 2007. Nonparametric statistical testing of EEG- and MEG-data. Manda Fischer: Conceptualization, Methodology, Software, Formal J. Neurosci. Methods 164 (1), 177–190. https://doi.org/10.1016/j. analysis, Investigation, Writing - original draft, Writing - review & jneumeth.2007.03.024. Mazza, V., Turatto, M., Umilta, C., 2005. Foreground-background segmentation and editing, Visualization, Project administration. Morris Moscovitch: attention: a change blindness study. Psychol. Res. 69, 201–210. https://doi.org/ Conceptualization, Methodology, Resources, Writing - review & editing, 10.1007/s00426-004-0174-9. Supervision, Project administration, Funding acquisition. Claude Alain: Mograss, M., Godbout, R., Guillem, F., 2006. The ERP old-new effect: a useful indicator in studying the effects of sleep on memory retrieval processes. Sleep 29 (11), Conceptualization, Methodology, Resources, Data curation, Writing - 1491–1500. https://doi.org/10.1093/sleep/29.11.1491. review & editing, Supervision, Project administration, Funding Moscovitch, M., 1992. Memory and working with memory: a component process model acquisition. based on modules and central systems. J. Cognit. Neurosci. 4, 257–267. Moscovitch, M., 2007. Why the engram is elusive: memory does not exist until it is recovered. In: Tulving, E., Roediger III, H.L., Dudai, Y., Fitzpatrick, S.M. (Eds.), Declaration of competing interest Science of Memory: Concepts. Oxford University Press, Oxford, UK, pp. 17–22. Moscovitch, M., Cabeza, R., Winocur, G., Nadel, L., 2016. Episodic memory and beyond: the Hippocampus and neocortex in transformation. Annu. Rev. Psychol. 67, None. 105–134. https://doi.org/10.1146/annurev-psych-113011-143733. Nabeta, T., Ono, F., Kawahara, J., 2003. Transfer of spatial context from visual to haptic Acknowledgements search. Perception 32, 1351–1358. https://doi.org/10.1068/p5135. Nakayama, K., Shimojo, S., Silvermann, G.H., 1989. Stereoscopic depth: its relation to image segmentation, grouping, and the recognition of occluded objects. Perception We thank Vanessa Chan, Karishma Ramdeo, and Shahier Paracha for 18, 55–68. https://doi.org/10.1068/p180055. their assistance. We would also like to thank the editor and anonymous Ostergaard, A.L., 1992. A method for judging measures of stochastic dependence: further comments on the current controversy. J. Exp. Psychol. Learn. Mem. Cognit. 18, reviewers for their very thoughtful and helpful input. 413–420. https://doi.org/10.1037/0278-7393.18.2.413. Paller, K.A., Kutas, M., McIsaac, H.K., 1998. An electrophysiological measure of priming References of visual word- form. Conscious. Cognit. 7, 54–66. Pichora-Fuller, K.M., Alain, C., Schneider, B., 2017. Older adults at the cocktail party. In: Middlebrook, J.C., Simon, J.Z., Popper, A.N., Fay, R.F. (Eds.), The Auditory System Aine, C.J., Supek, S., George, J.S., 1995. Temporal dynamics of visual-evoked at the Cocktail Party. Springer, pp. 227–259. https://doi.org/10.1007/978-3-319- neuromagnetic sources: effects of stimulus parameters and selective attention. Int. J. 51662-2_9. Neurosci. 80, 79–104. Patai, E.Z., Doallo, S., Nobre, A.C., 2012. Long-term memories bias sensitivity and target Alain, C., Bernstein, L.J., 2015. Auditory scene analysis: tales from cognitive selection in complex scenes. J. Cognit. Neurosci. 24, 2281–2291, 10. 1162/jocn_a_ neurosciences. Music Perception 33, 70–82. 00294. Alain, C., Du, Y., Bernstein, L.J., Barten, T., Banai, K., 2018. Listening under difficult Plaut, D.C., 1995. Double dissociation without modularity: evidence from connectionist conditions: an activation likelihood estimation meta-analysis. Hum. Brain Mapp. 39, neuropsychology. J. Clin. Exp. Neuropsychol. 17, 291–321. https://doi.org/ 2695–2709. https://doi.org/10.1002/hbm.24031. 10.1080/01688639508405124. Assumpçao,˜ L., Shi, Z., Zang, X., Müller, H.J., Geyer, T., 2015. Contextual cueing: Poldrack, R.A., Selco, S.L., Field, J.E., Cohen, N.J., 1999. The relationship between skill implicit memory of tactile context facilitates tactile search. Atten. Percept. learning and repetition priming: experimental and computational analyses. J. Exp. Psychophys. 77 (4), 1212–1222. https://doi.org/10.3758/s13414-015-0848-y. Psychol. Learn. Mem. Cognit. 25, 208–235. https://doi.org/10.1037//0033- Awh, E., Jonides, J., 2001. Overlapping mechanisms of attention and spatial working 295X.109.2.401. memory. Trends Cognit. Sci. 5, 119–126. Pollmann, S., Manginelli, A.A., 2009. Early implicit contextual change detection in Backer, K.C., Alain, C., 2013. Attention to memory: orienting attention to sound object anterior prefrontal cortex. Brain Res. 1263, 87–92. https://doi.org/10.1016/j. representations. Psychol. Res. 78 (3) https://doi.org/10.1007/s00426-013-0531-7. brainres.2009.01.039. Backer, K.C., Binns, M.A., Alain, C., 2015. Neural dynamics underlying attentional Reingold, E.M., Merikle, P.M., 1990. On the inter-relatedness of theory and measurement orienting to auditory representations in short-term memory. J. Neurosci. 35 (3), in the study of unconscious processes. Mind Lang. 5, 9–28. 1307–1318. https://doi.org/10.1523/JNEUROSCI.1487-14.2015. Romero, K., Moscovitch, M., 2015. Amnesia: general. In: Wright, J.D. (Ed.), International Bae, G., Luck, S., 2017. Dissociable decoding of spatial attention and working memory Encyclopedia of the Social and Behavioral Sciences, second ed. Elsevier Ltd, UK, from EEG oscillations and sustained potentials. J. Neurosci. 38 (2), 409–422. https:// pp. 644–650. doi.org/10.1523/JNEUROSCI.2860-17, 2860-17. Rugg, M.D., Curran, T., 2007. Event-related potentials and recognition memory. Trends Bregman, A.S., 1990. Auditory Scene Analysis: the Perceptual Organization of Sound. Cognit. Sci. 11, 251–257. https://doi.org/10.1016/j.tics.2007.04.004. MIT Press, Cambridge, MA. Rugg, M.D., Mark, R.E., Walla, P., Schloerscheidt, A.M., Birch, C.S., Allen, K., 1998. Chun, M.M., Jiang, Y., 1998. Contextual cueing: implicit learning and memory of visual Dissociation of the neural correlates of implicit and explicit memory. Nature 392 context guides spatial attention. Cognit. Psychol. 7 (36), 28–71. https://doi.org/ (6676), 595–598. https://doi.org/10.1038/33396. 10.1006/cogp.1998.0681.

11 M. Fischer et al. Neuropsychologia 147 (2020) 107586

Schacter, D.L., Dobbins, I.G., Schnyer, D.M., 2004. Specificity of priming: a cognitive Trick, L., Enns, J., Mills, J., Vavrik, J., 2004. Paying attention behind the wheel: a neuroscience perspective. Nat. Rev. Neurosci. 5, 853–862. https://doi.org/10.1038/ framework for studying the role of attention in driving. Theor. Issues Ergon. Sci. 5 nrn1534. (5), 385–424. https://doi.org/10.1080/14639220412331298938. Schacter, D.L., Wig, G.S., Stevens, W.D., 2007. Reductions in cortical activity during Vilberg, K.L., Moosavi, R.F., Rugg, M.D., 2006. The relationship between priming. Curr. Opin. Neurobiol. 17, 171–176. electrophysiological correlates of recollection and amount of information retrieved. Schneider, W., Shiffrin, R.M., 1977. Controlled and automatic human information Brain Res. 1122, 161–170. https://doi.org/10.1016/j.brainres.2006.09.023. processing: I. Detection, search and attention. Psychol. Rev. 84, 1–66. Vilberg, K.L., Rugg, M.D., 2007. Dissociation of the neural correlates of recognition Shanks, D.R., 2005. Implicit learning. In: Lamberts, K., Goldstone, R.L. (Eds.), Handbook memory according to familiarity, recollection, and amount of recollected of Cognition. SAGE Publications Ltd, London, pp. 202–220. https://doi.org/ information. Neuropsychologia 45 (10), 2216–2225. https://doi.org/10.1016/j. 10.4135/9781848608177. neuropsychologia.2007.02.027. Shanks, D.R., St John, M.F., 1994. Characteristics of dissociable human learning systems. Wilding, E.L., 2000. In what way does the parietal ERP old/new effect index Behav. Brain Sci. 17, 367–447. recollection? Int. J. Psychophysiol. 35, 81–87. https://doi.org/10.1016/S0167-8760 Shulman, G.L., Astafiev,S.V., McAvoy, M.P., d’Avossa, G., Corbetta, M., 2007. Right TPJ (99)00095-1. deactivation during visual search: functional significance and support for a filter Wolfe, J.M., 2003. Moving towards solutions to some enduring controversies in visual hypothesis. Cerebr. Cortex 17, 2625–2633. https://doi.org/10.1093/cercor/bhl170. search. Trends Cognit. Sci. 7 (2) https://doi.org/10.1016/S1364-6613(02)00024-4. Snyder, J.S., Gregg, M.K., 2011. Memory for sound, with an ear toward hearing in Wolters, G., Prinsen, A., 1997. Full versus divided attention and implicit memory complex auditory scenes. Atten. Percept. Psychophys. 73 (7), 1993–2007. https:// performance. Mem. Cognit. 25 (6), 764–771. https://doi.org/10.3758/BF03211319. doi.org/10.3758/s13414-011-0189-4. Zang, X., Geyer, T., Assumpçao,˜ L., Müller, H.J., Shi, Z., 2016. From foreground to Thompson, C., Sabik, M., 2018. Allocation of attention in familiar and unfamiliar traffic background: how task-neutral context influences contextual cueing of visual search. scenarios. Transport. Res. F Traffic Psychol. Behav. 55, 188–198. https://doi.org/ Front. Psychol. 7 (852) https://doi.org/10.3389/fpsyg.2016.00852. 10.1016/j.trf.2018.03.006. Zimmermann, J.F., Moscovitch, M., Alain, C., 2017. Long-term memory biases auditory Tolman, E.C., 1948. Cognitive maps in rats and men. Psychol. Rev. 55, 189–208. spatial attention. J. Exp. Psychol. Learn. Mem. Cogn. 43 (10) https://doi.org/ Treisman, A.M., Gelade, G., 1980. A feature-integration theory of attention. Cognit. 10.1037/xlm0000398}. Psychol. 12, 97–136. Zimmermann, J., Ross, B., Moscovitch, M., Alain, C., 2020. Neural dynamics supporting auditory long-term memory effects on target detection. Neuroimage 218, 116979. https://doi.org/10.1016/j.neuroimage.2020.116979.