The special role of item context associations in the direct-access region of working memory

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1 DOI /s ORIGINAL ARTICLE The special role of item context associations in the direct-access region of working memory Guillermo Campoy 1 Received: 28 December 2015 / Accepted: 21 July 2016 Springer-Verlag Berlin Heidelberg 2016 Abstract The three-embedded-component model of working memory (WM) distinguishes three representational states corresponding to three WM regions: activated long-term memory, direct-access region (DAR), and focus of attention. Recent neuroimaging research has revealed that access to the DAR is associated with enhanced hippocampal activity. Because the hippocampus mediates the encoding and retrieval of item context associations, it has been suggested that this hippocampal activation is a consequence of the fact that item context associations are particularly strong and accessible in the DAR. This study provides behavioral evidence for this view using an itemrecognition task to assess the effect of non-intentional encoding and maintenance of item location associations across WM regions. Five pictures of human faces were sequentially presented in different screen locations followed by a recognition probe. Visual cues immediately preceding the probe indicated the location thereof. When probe stimuli appeared in the same location that they had been presented within the memory set, the presentation of the cue was expected to elicit the activation of the corresponding WM representation through the just-established item location association, resulting in faster recognition. Results showed this same-location effect, but only for items that, according to their serial position within the memory set, were held in the DAR. & Guillermo Campoy gcampoy@um.es 1 Universidad de Murcia, Facultad de Psicología, Campus de Espinardo, Murcia, Spain Introduction A number of important complex cognitive activities (such as reasoning, planning, or language comprehension) depend on our capacity to maintain a small number of mental representations readily available for current processing. The terms working memory (WM) and short-term memory (STM) are used to refer to the memory system underlying this capacity. 1 Traditional models (Atkinson & Shiffrin, 1968; Baddeley & Hitch, 1974) posited that WM relies on specialized memory stores that are structurally different from those sustaining long-term memory (LTM). From an alternative view, WM and LTM share the same representational substrate, but WM representations are in a particular state that gives them privileged accessibility for processing (Cowan, 1995; Oberauer, 2002, 2009; Ruchkin, Grafman, Cameron, & Berndt, 2003). Within this second approach, the threeembedded-component model (Oberauer, 2002, 2009) distinguishes three states of representations, which correspond to what is metaphorically described as three different regions of WM: the activated part of LTM (altm), the direct-access region (DAR), and the focus of attention (FA). According to the model, information in the altm is not immediately available for processing, but can be straightaway selected into a more central region, the DAR. 1 STM can be conceived as the expression of the WM system in situations in which performance does not significantly depend on the executive control mechanisms that generally play a decisive role in more prototypical WM tasks. From this perspective, WM represents a wider and more inclusive concept and that is why I will use this term throughout the paper. In any case, it is important to note that this study does not focus on the attentional mechanisms of executive control that makes WM different from STM, but on the memory component of WM, what Oberauer (2009) calls declarative WM.

2 The DAR can hold a limited number of representations, which constitute the candidate set for the FA. The FA selects a single representation at a time as the target for the upcoming mental operation. In a recent study, Nee and Jonides (2013) provided neuroimaging evidence for the Oberauer s model in the visual domain using functional magnetic resonance imaging (fmri) while participants performed an item-recognition task (Sternberg, 1966). Each trial began with the sequential presentation of five pictures of human faces (the memory set) in five different screen locations. Then, a probe face was presented and participants had to respond as to whether this probe was positive or negative. Positive probes matched a face in the memory set whereas negative probes did not. Because probes appeared immediately after the presentation of the last item of the memory set, the WM representation for this item was assumed to reside in the FA at the moment of testing. The DAR presumably retained representations for the items immediately preceding the last one, whereas representations for the first items of the sequence were assumed to have been relegated to the altm. Thus, the serial position in which positive probes had appeared during the presentation of the memory set determined which of the three WM regions was being tested in a given trial (Nee & Jonides, 2011; Öztekin, Davachi, & McElree, 2010). Neuroimaging data revealed a triple dissociation: testing the FA resulted in the selective activation of the inferior parietal cortex, access to information in the DAR was related to activation of the right hippocampus, and retrieval from the altm involved activation of the left ventrolateral prefrontal cortex (for similar findings in the verbal domain, see Nee & Jonides, 2011). The present study was aimed to examine a possible explanation for the increased hippocampal activity during DAR access: that this hippocampal activity was a consequence of the special role of item context associations in the DAR (Nee & Jonides, 2013). This explanation rests on the model of medial temporal lobe organization proposed by Eichenbaum and coworkers (Eichenbaum, Sauvage, Fortin, Komorowski, & Lipton, 2012; Eichenbaum, Yonelinas, & Ranganath, 2007). According to this model, neocortical inputs conveying information about item features (the what processing stream) converge in the perirhinal cortex and lateral entorhinal area, whereas inputs regarding item location (the where stream) converge in the parahippocampal cortex and medial entorhinal area. Importantly, these two processing streams remain largely parallel until both converge in the hippocampus. For this reason, the hippocampus plays the central role in the formation and maintenance of item context associations (Eichenbaum et al., 2007, 2012). On the other hand, an important assumption in the Oberauer s model of WM is that information held in the DAR is integrated into structures by the temporal binding of item and context representations (Oberauer, 2009). As far as the hippocampus mediates this item context binding, hippocampal activity in the study by Nee and Jonides (2013) could be a consequence of the selective activation of hippocampal relational representations when probes matched an item in the DAR. The present experiment provides behavioral evidence for this account by demonstrating a selective effect of item context associations for the items whose representations are presumably held in the DAR. The procedure here was equivalent to that employed by Nee and Jonides (2013) with two key modifications. First, whereas in Nee and Jonides (2013) positive probes appeared in the same spatial location as they had been presented within the memory set, this occurred on only half the trials in the present experiment (same-location condition); on the other half (different-location condition), positive probes were presented in a neutral position in which no member of the memory set had appeared (the center of the display). Second, the probe stimulus was immediately preceded by a visual cue indicating the location in which the probe was about to appear. Importantly, the location of the cue (and the subsequent probe) had no predictive value because positive and negative probes appeared equally often in each of the six test locations. The expectation was that the presentation of the spatial cue in positive-probe trials would activate the representation of the item presented in that position through the just-established item context association. This would result in shorter reaction time (RT) for positive probes in the same-location condition than in the different-location condition (the same-location effect). However, on the basis of Nee and Jonides (2013), it was also expected a modulation of the effect as a function of serial position, with the location effect being restricted to (or, at least, most pronounced for) probes that matched an item in the DAR. Method Participants Twenty-seven undergraduate students from the University of Murcia (17 women and 10 men; M age = 21.5 years, SD = 3.3) participated for course credit. The number of participants was determined in advance, and all participants were tested before starting data analysis. Materials Two hundred and twenty color pictures of human faces (half female, half male) were selected from the Glasgow Unfamiliar Face Database (Burton, White, & McNeill,

3 2010). Faces had neutral expression and were of similar age and race (Caucasian). They were devoid of glasses or piercings. A different group of faces from the same database was used for practice trials. A computer program generated by E-Prime (Schneider, Eschman, & Zuccolotto, 2002) controlled the experiment. Stimuli were presented on a TFT monitor and responses were collected via keyboard. The basic display, which remained visible throughout each trial, consisted of five rectangular presentation boxes (175 pixels wide by 250 pixels high; equivalent to 5.1 cm by 7.3 cm) arranged at regular intervals along an imaginary semicircle (radius = 488 pixels, equivalent to 14.3 cm). A black plus sign marked the center of this semicircle. Presentation boxes were white color, with a black border of one pixel width. Screen background color was silver gray. Procedure Participants were tested individually in soundproof booths. The experimental procedure is depicted in Fig. 1. Each trial began with the presentation of the basic display described above for 1000 ms. Then, the five faces comprising the memory set were sequentially presented within the five boxes, starting from the leftmost presentation box. Each face was displayed for 1000 ms, and immediately followed by a 250-ms mask (a black rectangle entirely occupying the corresponding box). Next, after an interval of 250 ms, a visual cue was presented indicating the position of the forthcoming probe. The cue was displayed for 250 ms, and consisted of a rectangular box equivalent to the presentation boxes but with a black border of 15 pixels width. Cues appeared either over one of the five presentation boxes or in the center of the display (the position marked by the plus sign). After that, the probe face appeared in the cued location and participants indicated whether the probe matched a face in the memory set by pressing the Z or M key on the computer keyboard. Probes remained visible for 1500 ms or until response. Next, a feedback message ( correct!, error!, or too slow ) appeared for 500 ms. Finally, the screen went blank for 1000 ms, and a new trial began. Fig. 1 Schematic representation of the experimental procedure. The examples illustrated correspond to positive-probe trials

4 The experiment comprised eight blocks of 20 trials. Each block included 10 positive-probe trials representing all the combination of serial position (1 5) and probe position (same or different). In the same-position condition, probes appeared in their presentation box, whereas in the different-position condition, probes were presented in the central position. To avoid predictability, probe positions in the ten negative-probe trials of each block replicated those in positive-probe trials. Thus, within each block, one negative probe was presented in each of the five presentation boxes and five negative probes appeared in the central location. The order of the trials in each block was randomized. Within a block, all the faces were of the same gender, with each face of the pertinent gender appearing in only one trial per block. Male-face and female-face blocks were run alternatively, so that participants completed at least a full block before a face presented in a previous trial appeared now as a negative probe. This was intended to minimize the levels of proactive interference in negativeprobe trials (Campoy, 2011; Jonides & Nee, 2006). Participants completed 16 practice trials before the experimental trials. Results Nee and Jonides (2013) used Cowan s K (Cowan, 2001), calculated by the formula K = 5 9 (proportion of hits - proportion of false alarms), to estimate DAR capacity for each participant and individually assign serial positions to WM regions. Using rounded values, they assigned serial positions 1 to K - 1 to reflect retrieval from altm, the K - 1 serial positions immediately preceding the last one to reflect DAR access, and the last serial position (serial position 5) to reflect access to the FA. Following the same logic, and to allow direct comparison, Cowan s K was calculated for each participant and serial positions were individually assigned to WM regions. In this calculation, I only used data from the trials of the samelocation condition, that is, the trials that were equivalent to those in the study by Nee and Jonides (for a discussion of why it might be inappropriate to include trials of the different-location condition to calculate Cowan s K, see Li, Cowan, & Saults, 2013). 2 K ranged from 2.20 to 4.05, with a mean of 3.22 (SD = 0.43). Serial positions assigned to reflect DAR access were positions 2 4 for seven participants, positions 3 and 4 for 19 participants, and position 4 for one participant. In the analyses described below, serial position is entered as a factor first. Then, an equivalent analysis is performed after individually aggregating serial positions into WM regions. 2 I thank an anonymous reviewer for this observation. To analyze participants accuracy in discriminating between positive and negative probes, A 0 values were calculated from the proportion of hits and false alarms in each condition. This discrimination index ranged from 0 to 1, with A 0 = 1 indicating perfect performance in the recognition task and A 0 = 0.5 representing absence of discrimination (Pollack & Norman, 1964). As shown in Fig. 2, A 0 values were clearly above the 0.5 level, revealing good discrimination across serial positions and WM regions. Mean A 0 values were submitted to a within-subjects analysis of variance (ANOVA) with serial position (1 5) and probe location (same or different) as factors. There was a main effect of serial position, F(4, 104) = 31.97, MSE = , p \ 0.001, g p 2 = 0.55, revealing better discrimination as we move forward along serial positions. Post hoc Bonferroni tests (MSE = ; df = 104) showed significant differences between each two consecutive positions (all ps \ 0.022) except between serial position 1 and 2 (p = 1). Although there was a tendency for better performance in the same-location condition for all serial positions except the first, neither the main effect of probe location nor the interaction reached statistical significance, F(1, 26) = 2.29, MSE = , p = 0.142, g p 2 = 0.08, and F(4, 104) \ 1, respectively. Mean A 0 values were also submitted to a within-subjects ANOVA with WM region (altm, DAR, and FA) and probe location (same or different) as factors. There was a main effect of WM region, F(2, 52) = 76.71, MSE = , p \ 0.001, g p 2 = 0.75, with post hoc Bonferroni tests (MSE = ; df = 52) revealing significant differences between each two consecutive regions (all ps \ 0.001). Neither the main effect of probe location nor the interaction reached statistical significance, F(1, 26) = 2.71, MSE = , p = 0.112, g p 2 = 0.09, and F(2, 52) \ 1, respectively. The analyses of interest, however, were those involving participants RT on positive-probe trials. For these analyses, trials with incorrect responses (14.63 %) and trials with no response (0.65 %) were excluded. Inspection of RTs revealed no outliers, defined as RTs shorter than 200 ms or diverging from the individual participants mean in the corresponding condition by more than three standard deviations. Figure 3a shows the mean RTs on positiveprobe trials as a function of serial position and probe location (see also Table 1). To better appreciate the main finding of this study, Fig. 3b depicts the location effect (RT on different-location trials minus RT on same-location trials) as a function of serial position. According to expectations, Fig. 3 reveals a clear location effect in serial position 3 and 4, with the effect being reduced or eliminated in the rest of serial positions. Congruently, a 5 (serial position) 9 2 (probe location) within-subjects ANOVA showed a main effect of location, F(1, 26) = 5.837, MSE = , p = 0,023, g p 2 = 0.183, revealing shorter

5 Fig. 2 Mean A 0 discrimination values across serial positions (a) and working memory regions (b). Error bars represent 95 % confidence intervals (calculated according to Masson and Loftus, 2003) Fig. 3 Mean RTs (a) and location effect (b) across serial positions. Error bars represent 95 % confidence intervals (calculated according to Masson and Loftus, 2003) Table 1 Mean reaction times for correct responses across serial positions (SP) and working memory regions (standard deviations in parentheses) Probe location SP 1 SP 2 SP 3 SP 4 SP 5 altm DAR FA Same 859 (122) 836 (127) 803 (132) 727 (114) 651 (100) 848 (114) 772 (105) 651 (100) Different 853 (119) 855 (113) 862 (144) 773 (99) 644 (94) 852 (105) 821 (112) 644 (94) RT for positive probes in the same-location condition than in the different-location condition (the location effect). However, there was also an interaction between probe location and serial position, F(4, 104) = 3.341, MSE = , p = 0,013, g p 2 = Post hoc Bonferroni tests (MSE = , df = 104) revealed that correct responses on positive trials were faster in the same-location condition than in the different-location condition for items presented in serial positions 3 (p = 0.002) and 4 (p = 0.027), whereas there was no location effect for the other three serial positions (all ps = 1). The sizes of the location effects (Cohen s d) for serial position 1 5 were -0.05, 0.20, 0.69, 0.49, and -0.11, respectively. Figure 4 shows the mean RTs on positive-probe trials (panel A) and the location effect (panel B) across WM regions (see also Table 1). A 3 (WM region) 9 2 (probe

6 Fig. 4 Mean RTs (a) and location effect (b) across working memory regions. Error bars represent 95 % confidence intervals (calculated according to Masson and Loftus, 2003) location) within-subjects ANOVA showed an interaction between probe location and WM region, F(2, 52) = 5.306, MSE = , p = 0.008, g p 2 = Post hoc Bonferroni tests (MSE = , df = 52) revealed that correct responses on positive trials were faster in the same-location condition than in the different-location condition for DAR items (p = 0.001), whereas there was no location effect in the other WM regions (all ps = 1). The sizes of the location effects (Cohen s d) for altm, DAR and FA items were 0.05, 0.73, and -0.11, respectively. Discussion Although damage to the hippocampus results in severe impairment of declarative LTM, amnesic patients with hippocampal damage perform normally in a range of simple memory tasks involving immediate recall or recognition of digits, words, locations, etc. (e.g., Cave & Squire, 1992). This fact has led to the widespread view that WM does not rely on the hippocampus, and is frequently described as representing the clearest dissociation between WM and declarative LTM (Baddeley & Warrington, 1970; Cave & Squire, 1992; Squire & Wixted, 2011; Wickelgren, 1968). Over the last years, however, evidence is growing that the hippocampus could play a critical role in WM tasks when to-be-remembered material includes relational information, mainly item location associations (Braun et al. 2011; Olson, Page, Moore, Chatterjee, & Verfaellie, 2006; Pertzov et at., 2013; Watson, Voss, Warren, Tranel, & Cohen, 2013; Yee, Hannula, Tranel, & Cohen, However, see Allen, Vargha-Khadem, & Baddeley, 2014; Jeneson, Mauldin, Hopkins, & Squire, 2011). These observations have resulted in a debate between two alternative interpretations. On the one hand, it has been suggested that the hippocampus mediates the formation and maintenance of item context binding regardless the length of the retention interval, and not only in the long term. From this view, thus hippocampal associative mechanisms are naturally recruited by WM according to the demands of the task (Libby, Hannula, & Ranganath, 2014; Monti et al. 2015; Yonelinas, 2013). Others, on the other hand, consider that the hippocampus contributes to performance in WM tasks only when WM capabilities are exceeded and performance starts to depend on LTM; proper WM, however, does not actually rely on the hippocampus (Jeneson et al., 2011; Jeneson & Squire, 2012). Within this debate, neuroimaging results described by Nee and Jonides (2013) might be taken as evidence for the first of these two interpretations. In their study, Nee and Jonides (2013) presented five faces sequentially in different screen locations followed by an immediate probe recognition test, and examined the patterns of neuronal activity associated to the access to representations held in each of the three WM regions proposed by Oberauer (2002): altm, DAR, and FA. Hippocampal activation did not emerge when retrieved representations were those that had been displaced to the border region between WM and LTM (the altm), a finding that would be more congruent with the view that the hippocampus is only recruited by LTM processes. Instead of that, hippocampal activation was selectively elicited by positive probes that, according to its serial position within the memory set, matched a representation in a central region of WM: the DAR. This finding seems more compatible with the view that hippocampal mechanisms were naturally recruited during WM tasks as part of its putative processes.

7 Leaving aside this controversy, the question now is what could be the origin of the hippocampal activation found by Nee and Jonides (2013). As said, the hippocampus could play a critical role in the formation and maintenance of item context association (Eichenbaum et al., 2012). Thus, a tentative explanation is that, in contrast to probes tapping other WM regions, the presentation of DAR probes elicited the activation of these hippocampal relational representations (Nee and Jonides, 2013). This tentative account has the virtue of being congruent with the notion that a particular characteristic of the information held in the DAR is that representations are integrated into structures by item contexts associations, allowing immediate access by the focus of attention (Oberauer, 2009). Unfortunately, however, the procedure in the study of Nee and Jonides (2013) did not allow assessing whether item context associations were in fact particularly strong and accessible for the items held in the DAR. After modifying the original procedure, the present work complements the study of Nee and Jonides (2013) by providing behavioral evidence for the special role of item context associations in the DAR. In the experiment described, each probe was immediately preceded by a visual cue indicating the location of the screen in which the probe was about to appear. When positive probes were presented in the same location that they had appeared within the memory set (half of the trials), it was expected that, to the extent that item context associations were accessible, the presentation of the cue would lead to the activation of the corresponding WM representation through the item context link, resulting in faster recognition and shorter RTs. Thus, an inspection of the same-location effect across serial positions would reveal the strength and accessibility of the item context associations in each WM region. On the basis of Nee and Jonides (2013), the prediction was that the location effect would be especially pronounced for the items presumably maintained in the DAR, namely those immediately preceding the last stimulus within the memory set. As expected, data revealed a location effect that was confined to DAR items, confirming the prediction. This finding supports the notion that item context associations are especially important for representations held in the DAR, and are congruent with the suggestion that hippocampal activation selectively elicited by DAR probes in the study of Nee and Jonides (2013) was a consequence of the special role of these relational representations for DAR items. It is important to note that the same-location effect in this study was found in a situation in which participants have to attend to the identity of the probes, whereas their location was actually an irrelevant dimension. Consequently, there was no reason for the participants to intentionally encode and maintain item location associations. Moreover, the possibility that a negative probe had appeared in the immediately preceding trials was explicitly prevented (see Procedure section), what presumably minimized the familiarity of negative probes. In this situation, participants could rely on the level of familiarity without engaging in less automatic recollection mechanisms involving the use of relational item context information. Finally, a short stimulus-onset asynchrony (SOA) between cue and probe (250 ms) most probably prevents the participation of controlled processes that involved explicit, strategic use of information about cue location. Thus, it seems plausible that the same-location effect in this study was mainly a consequence of automatic rather than controlled processes. 3 Because of that, the procedure introduced here may represent a helpful alternative to those commonly employed to investigate the short-term maintenance of item location associations in hippocampal amnesia. In these studies, amnesic patients are explicitly instructed to maintain item location associations in memory for latter recall or recognition. The downside of this is that amnesic patients could tend to implement alternative non-relational strategies to satisfy task requirements despite their memory deficit (Clark & Maguire, 2016). The procedure introduced here may avoid this problem by evaluating unintentional encoding, maintenance and retrieval of item location associations in the short term. Compliance with ethical standards Funding This study was funded by the Spanish Ministry of Economy and Competitiveness (Project PSI P) and by the Agency for Science and Technology in the Region of Murcia (Seneca Foundation; project 19267/PI/14). Conflict of interest The author declares that he has no conflict of interest. Ethical approval All procedures performed were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent Informed consent was obtained from all individual participants included in the study. 3 Although this automatic, familiarity-based account seems plausible, alternative explanations cannot be ruled out. For example, participants could have strategically used item location information to reduce the size of the memory search set in the same-location condition, whereas search-set size in the different-location condition was always five (I thank an anonymous reviewer for pointing out this possibility). This would lead to faster RTs in the same-location condition when item location information was available. Importantly, the main conclusion from this view would remain the same because results would reveal that item location information was selectively available for DAR items.

8 References Allen, R. J., Vargha-Khadem, F., & Baddeley, A. D. (2014). Itemlocation binding in working memory: Is it hippocampusdependent? Neuropsychologia, 59, Atkinson, R. C., & Shiffrin, R. M. (1968). Human memory: A proposed system and its control processes. In K. W. Spence & J. T. Spence (Eds.), The psychology of learning and motivation: advances in research and theory (Vol. 2, pp ). New York: Academic Press. Baddeley, A. D., & Hitch, G. J. (1974). Working memory. In G. H. Bower (Ed.), The psychology of learning and motivation: Advances in research and theory (Vol. 8, pp ). New York: Academic. Baddeley, A. D., & Warrington, E. K. (1970). Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, Braun, M., Weinrich, C., Finke, C., Ostendorf, F., Lehmann, T. N., & Ploner, C. J. (2011). Lesions affecting the right hippocampal formation differentially impair short-term memory of spatial and nonspatial associations. Hippocampus, 21, Burton, A. M., White, D., & McNeill, A. (2010). The glasgow face matching test. Behavior Research Methods, 42, doi: /BRM Campoy, G. (2011). Retroactive interference in short-term memory and the word-length effect. Acta Psychologica, 138, Cave, C. B., & Squire, L. R. (1992). Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus, 2, Clark, I. A., & Maguire, E. A. (2016). Remembering preservation in hippocampal amnesia. Annual Review of Psychology, 67, Cowan, N. (1995). Attention and memory: an integrated framework. Oxford: Oxford University Press. Cowan, N. (2001). The magical number 4 in short-term memory: A reconsideration of mental storage capacity. Behavioral and Brain Sciences, 24, Eichenbaum, H., Sauvage, M., Fortin, N., Komorowski, R., & Lipton, P. (2012). Towards a functional organization of episodic memory in the medial temporal lobe. Neuroscience and Biobehavioral Reviews, 36, Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 152. Jeneson, A., Mauldin, K. N., Hopkins, R. O., & Squire, L. R. (2011). The role of the hippocampus in retaining relational information across short delays: The importance of memory load. Learning and Memory, 18, Jeneson, A., & Squire, L. R. (2012). Working memory, long-term memory, and medial temporal lobe function. Learning and Memory, 19, Jonides, J., & Nee, D. E. (2006). Brain mechanisms of proactive interference in working memory. Neuroscience, 139, Li, D., Cowan, N., & Saults, J. S. (2013). Estimating working memory capacity for lists of nonverbal sounds. Attention, Perception, & Psychophysics, 75, Libby, L. A., Hannula, D. E., & Ranganath, C. (2014). Medial temporal lobe coding of item and spatial information during relational binding in working memory. Journal of Neuroscience, 34, Masson, M. E. J., & Loftus, G. R. (2003). Using confidence intervals for graphically based data interpretation. Canadian Journal of Experimental Psychology, 57, Monti, J. M., Cooke, G. E., Watson, P. D., Voss, M. W., Kramer, A. F., & Cohen, N. J. (2015). Relating hippocampus to relational memory processing across domains and delays. Journal of Cognitive Neuroscience, 27, Nee, D. E., & Jonides, J. (2011). Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: Evidence for a 3-state model of memory. Neuroimage, 54, Nee, D. E., & Jonides, J. (2013). Neural evidence for a 3-state model of visual short-term memory. Neuroimage, 74, Oberauer, K. (2002). Access to information in working memory: Exploring the focus of attention. Journal of Experimental Psychology. Learning, Memory, and Cognition, 28, Oberauer, K. (2009). Design for a working memory. In B. H. Ross (Ed.), Psychology of learning and motivation: Advances in research and theory (Vol. 51, pp ). San Diego: Academic Press. Olson, I. R., Page, K., Moore, K. S., Chatterjee, A., & Verfaellie, M. (2006). Working memory for conjunctions relies on the medial temporal lobe. Journal of Neuroscience, 26, Öztekin, I., Davachi, L., & McElree, B. (2010). Are representations in working memory distinct from representations in long-term memory? Neural evidence in support of a single store. Psychological Science, 21, Pertzov, Y., Miller, T. D., Gorgoraptis, N., Caine, D., Schott, J. M., Butler, C., & Husain, M. (2013). Binding deficits in memory following medial temporal lobe damage in patients with voltagegated potassium channel complex antibody-associated limbic encephalitis. Brain, 136, Pollack, I., & Norman, D. A. (1964). A non-parametric analysis of recognition experiments. Psychonomic Science, 1, Ruchkin, D. S., Grafman, J., Cameron, K., & Berndt, R. S. (2003). Working memory retention systems: A state of activated longterm memory. Behavioral and Brain Sciences, 26, Schneider, W., Eschman, A., & Zuccolotto, A. (2002). E-Prime user s guide. Pittsburgh: Psychology Software Tools Inc. Squire, L. R., & Wixted, J. T. (2011). The cognitive neuroscience of human memory since H.M. Annual Review of Neuroscience, 34, Sternberg, S. (1966). High-speed scanning in human memory. Science, 153, Watson, P. D., Voss, J. L., Warren, D. E., Tranel, D., & Cohen, N. J. (2013). Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors. Hippocampus, 23, Wickelgren, W. A. (1968). Sparing of short-term memory in an amnesic patient: Implications for strength theory of memory. Neuropsychologia, 6, Yee, L. T. S., Hannula, D. E., Tranel, D., & Cohen, N. J. (2014). Short-term retention of relational memory in amnesia revisited: Accurate performance depends on hippocampal integrity. Frontiers in Human Neuroscience, 8, 16. Yonelinas, A. P. (2013). The hippocampus supports high-resolution binding in the service of perception, working memory and longterm memory. Behavioral Brain Research, 254,