Hitting the Reset Button an ERP Investigation of Memory For
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Brain Research 1642 (2016) 524–531 Contents lists available at ScienceDirect Brain Research journal homepage: www.elsevier.com/locate/brainres Research report Hitting the reset button: An ERP investigation of memory for temporal context Matthew M. Walsh a,b,n, Christopher A. Paynter a, Ya Zhang c, Lynne M. Reder a a Carnegie Mellon University, Pittsburgh, PA, United States b TiER1 Performance Solutions, Cincinnati, OH, United States c University of Pittsburgh, Pittsburgh, PA, United States article info abstract Article history: This study explored how temporal context influences recognition. In an ERP experiment, subjects were Received 2 September 2015 asked to judge whether pictures, presented one at a time, had been seen since the previous appearance Received in revised form of a special reset screen. The reset screen separated sequences of successively presented stimuli and 14 April 2016 signaled a change in temporal context. A “new-repeat” picture was one that had been seen before but was Accepted 19 April 2016 to be called “new” because it had not appeared since the previous reset screen. New-repeat pictures Available online 21 April 2016 elicited a more negative FN400 component than did “old” pictures even though both had seen before Keywords: during the experiment. This suggests that familiarity, as indexed by the FN400, is sensitive to temporal Recognition context. An earlier frontopolar old/new effect distinguished pictures that were seen for the first time in ERP the experiment from all other pictures. The late positive component (LPC), which is typically greater for Familiarity old stimuli, was smaller for new-repeat pictures than for pictures seen for the first time in the experi- Recollection FN400 ment. Finally, individual differences in task performance were predicted by the differences in amplitude LPC of P3b that was evoked by the onset of the reset screen. P3b & 2016 Published by Elsevier B.V. 1. Introduction contextual information (Curran, 2000; Duzel et al., 1997; Rugg and Yonelinas, 2003). Studies of memory using event-related potentials (ERPs) have In most dual-process models of recognition memory, famil- revealed two distinct ERP correlates of recognition. One of these is iarity is not sensitive to the context in which an item appeared the FN400, a negative deflection at frontal sites from 300 to (e.g. Diana et al., 2007; Eichenbaum et al., 2007; Jacoby, 1991; 500 ms, which is more negative for items judged new than for Montaldi and Mayes, 2010; Parks and Yonelinas, 2007; Reder et al., items judged old (Curran, 2000; Curran and Cleary, 2003; Duzel 2000; Yonelinas, 2002). However, there is some debate, even et al., 1997; Rugg and Curran, 2007; Rugg and Yonelinas, 2003; among dual-process theorists, about whether contextual in- Tsivilis et al., 2001; Yovel and Paller, 2004). The other is the late formation might contribute to familiarity in some circumstances. positive component (LPC), a positive deflection at parietal sites Some have suggested, for example, that familiarity is sensitive to the slowly changing global context defined by the experimental from 400 to 800 ms, which is more positive for items judged old setting (Mandler, 1980). In most studies of recognition memory, than for items judged new (Curran, 2000; Curran and Cleary, participants are asked to judge whether commonplace items were 2003; Duzel et al., 1997; Rugg and Curran, 2007; Rugg and Yone- encountered during the experiment. Familiarity judgments along linas, 2003; Tsivilis et al., 2001; Yovel and Paller, 2004). A common with the FN400 differ for old and new items, though all of the view in the literature is that these two components correspond to items have likely been encountered many times before the qualitatively distinct recognition memory processes (Rugg and experiment. Curran, 2007). The FN400 corresponds to a familiarity process that Behavioral work has shown that familiarity is also sensitive to provides information about whether an item has been seen, but local context (i.e., features that may vary from trial to trial). Pre- not the context in which it appeared. In contrast, the LPC corres- senting contextual features at test that have been seen repeatedly ponds to a recollection process that does involve retrieval of with other items during study increases spurious familiarity judgments (Diana et al., 2004). Additionally, instructing people to n encode contextual information along with items in a way that Correspondence to: Carnegie Mellon University, 5000 Forbes Avenue, Baker Hall, 455G, Pittsburgh, PA 15213, United States. promotes unitization increases the impact of context on familiarity E-mail address: [email protected] (M.M. Walsh). judgments (Diana et al., 2008, 2011). http://dx.doi.org/10.1016/j.brainres.2016.04.047 0006-8993/& 2016 Published by Elsevier B.V. M.M. Walsh et al. / Brain Research 1642 (2016) 524–531 525 The ERP methodology has been used to provide converging new, even if the picture had appeared several times in the pre- evidence that local context impacts familiarity. According to one vious block of trials. The perirhinal cortex is thought to be involved theory (Ecker et al., 2007a, 2007b), intrinsic (intra-item) con- in familiarity processing (see Diana et al. (2007) and Eichenbaum textual features such as object color are automatically processed et al. (2007) for reviews), and has been identified as a potential and bound to object tokens, whereas extrinsic features such as source of the FN400 (Curran et al., 2006; but see Rugg and Curran background shape are not (for a review, see Zimmer and Ecker (2007) for an alternate view). On the basis of those results, we (2010)). The absence of a match between the current stimulus and hypothesized that the FN400 in humans would also be sensitive to stored object tokens produces an FN400. Consequently, the FN400 when a stimulus last appeared relative to a signal that denoted the is only sensitive to intrinsic local context. In an experiment that start of a new block of trials. tested this theory, participants studied items presented in various In our modified version of the delayed-match-to-sample task, colors (Ecker et al., 2007a). At test, items appeared in the same subjects viewed a series of pictures of everyday items, along with color or in a different color. Subjects were asked to judge whether an occasional “reset” screen. With each presentation, they judged they had studied the object, ignoring its color. The FN400 was whether the picture had appeared since the most recent reset more negative when objects appeared in a different color than screen. The trials of greatest interest were those where a picture when they appeared in the same color. In a second condition of the that had appeared before was shown for the first time in the experiment, participants studied items presented on different current block of trials (i.e. new-repeats). The key question was background shapes. The manipulation of item-shape match during whether the FN400 to new-repeats would differ from the FN400 the test phase did not affect the FN400. Ecker et al. interpreted to other pictures that had already appeared in the current block of these results in terms of the differential impact of intrinsic and trials (i.e. old pictures). Both types of pictures had appeared in the extrinsic local context on familiarity processing. global context established by the experimental setting, but new- Subsequent studies have identified other contextual features repeats had not appeared since the reset screen. Therefore, if the that do and do not affect familiarity. The FN400 is sensitive to FN400 were more negative for new-repeat pictures than for old changes from study to test in object color (Ecker et al., 2007a), pictures, it would indicate that this component is sensitive to word font color (Nyhus and Curran, 2009), and object screen lo- temporal context. cation (Speer and Curran, 2007). The FN400 does not appear to be sensitive to the presence of a background shape (Ecker et al., 2007a), border color (Ecker et al., 2007a; Speer and Curran, 2007), 2. Results or superposition of an object upon a background image (Ecker et al., 2007b). Some of these results can be understood in terms of 2.1. Behavioral analyses the distinction between intrinsic and extrinsic local context. However, it is often difficult to define which features are intrinsic Response accuracy and correct response times are shown in and extrinsic to a stimulus in advance. Table 1. A repeated measures ANOVA revealed a significant dif- ference in accuracy across the four picture types, F(3, 57)¼30.50, 1.1. Is the FN400 sensitive to temporal context? po.001. Subjects responded more accurately to new-first pictures than to all other pictures (all po.001). Response accuracy did not Given that familiarity and the FN400 are influenced by at least vary across the remaining picture types (all p4.05). An ANOVA for some sources of contextual information, we asked whether the correct response times also revealed a main effect of picture type F FN400 is sensitive to temporal context. We manipulated temporal (3, 57)¼15.28, po.001. Responses to new-first and new-repeat context by presenting participants with sequences of images and pictures were slower than responses to old-first and old-repeat occasionally inserting a boundary – in the form of a “reset” screen – pictures (all po.01). Response durations did not different between between successive images. Participants were asked to judge new-first and new-repeat pictures, t(19)¼.43, p4.1, nor between whether each image had appeared since the last reset screen. old-first and old-repeat pictures, t(19)¼1.98, p4.05. Thus, the task involved location-based (i.e. temporal position re- lative to a boundary) rather than distance-based (i.e.