Electrophysiological Measures of Episodic Memory Control and Memory Retrieval
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1 Electrophysiological Measures of Episodic Memory Control and Memory Retrieval E. L. Wilding and J. E. Herron Key Words Episodic Memory Event-Related Potentials Recollection Retrieval Retrieval Mode Retrieval Orientation ABSTRACT Event-related potentials (ERPs) index processes that occur before, during and after retrieval of information from episodic memory. In this selective review we provide a loose theoretical framework within which retrieval processes operating at these different stages can be considered. We go on to describe how ERPs have been employed in order to index processes operating at each of these stages. These data have contributed to current understanding of the processes that are engaged around the time of episodic memory retrieval, and also illustrate the potential that ERPs have for understanding in detail how memory retrieval processes changes in populations with memory impairments. INTRODUCTION To remember an event, information must be retrieved from episodic memory. It is generally assumed that a key element in this process is an interaction between a memory trace and a retrieval cue. 1,2 According to most current accounts, memory traces are represented partially in neocortex, with the specific neocortical regions determined by the content of memories. 3-5 The retrieval cue is a mental representation that is generated internally. In most labbased tasks this cue is generated in response to an environmental stimulus, such as a word presented during a verbal memory task. Common to several models of episodic retrieval is the view that processes operating before as well as after cuetrace interactions determine what information is made available from memory and what information is employed to guide behavior. 6-9 The general notion is that processes engaged prior to the cue-trace interaction can influence the nature of that interaction, while processes acting after or in parallel with the interaction operate on the consequences of the interaction in service of task demands. According to this framework, retrieval failures and memory deficits can come about because of problems at different processing stages. Evidence consistent with this view comes from patients with selective brain damage who show deficits restricted to post-retrieval processing stages (for reviews see, 10,11 ) as well as from patients who have deficits that are assumed to originate prior to the cue-trace interaction. 12 In this article we review selectively recent research into episodic memory retrieval in which event-related potentials (ERPs) have been employed. The findings in these studies demonstrate that ERPs index three classes of retrieval process. First, preparatory processes that are engaged prior to retrieval and which influence the processes set in train when a retrieval cue is encountered. Second, retrieval attempts : processes initiated in response to a retrieval-cue and engaged in pursuit of retrieval. Third, retrieval success operations: processes engaged during and as a consequence of the cue-trace interaction. The fact that ERPs provide multiple indices of retrieval processes is important because this means that they can provide insights into the nature and function of the processes that are engaged at different memory processing stages. 13 Identification of electrophysiological markers for distinct classes of retrieval process is also a precursor to employing these as a means of determining how episodic memory is affected by factors such as age, disease state, and focal brain damage. In the remainder of this review we introduce recent findings that provide examples of how ERPs have been employed in order to understand the stages that are involved in episodic retrieval. We also comment on how this work can be or has been extended in order to understand memory retrieval processing and how it might break down in different populations. Pre-retrieval ( preparatory ) processes Tulving 14 introduced the concept of retrieval mode a cognitive set, entry into which ensures that subsequent E. L. Wilding and J. E. Herron are from the School of Psychology, Cardiff University, Cardiff, Wales, UK. Address requests for reprints to Dr. Ed Wilding, School of Psychology, Cardiff University, Cardiff, CF10 3AT, Wales, UK. This work was supported by the UK BBSRC and by the Wellcome Trust. wildinge@cardiff.ac.uk 315
2 Figure 1. (A). Grand average ERPs separated according to preparatory cue-type at leftand right-hemisphere frontal (F5/F6) and central (C5/C6) electrode locations. (B). Maps showing the differences between the scalp distributions of the ERPs associated with each pair of preparatory cues on stay trials over the ms epoch. The maps were computed from difference scores obtained by subtracting the ERPs evoked in one condition from those in another, as indicated above each map. The paired values below each map denote the maxima and minima of the amplitude differences between conditions. For example, for the left-most map, white denotes 1.4 µv, while black denotes -0.6 µv. This is a modified version of a figure presented by Herron and Wilding. 16 stimuli will be treated as episodic retrieval cues. A related concept, retrieval orientation, was discussed recently by Rugg and Wilding. 8 A retrieval orientation is a task-specific retrieval set, entry into which will ensure that subsequent stimuli are treated as retrieval cues for particular kinds of episodic information. 15 Thus an orientation is a more constrained retrieval set than is retrieval mode. Both mode and orientation are tonic states that can be maintained for as long as episodic retrieval is required, and can be observed with measures of brain activity that permit sustained or relatively slow changes in neural activity to be monitored. 8 ERPs fulfil this criterion, and in one recent study, Herron and Wilding 16 provided electrophysiological data demonstrating that retrieval mode may be common to all episodic tasks, while different retrieval orientations are adopted according to specific task demands. Participants were cued trial-by-trial to prepare for either a semantic retrieval task (judge whether individually presented words refer to a moving or a non-moving object) or one of two episodic retrieval tasks (remember spatial location or remember encoding operations). On each trial, ERPs were recorded time-locked to the preparatory cues indicating which task to prepare for, and the items requiring memory judgments (the retrieval cues) were presented 2s later. Participants made accurate memory judgments despite the requirements to switch between preparing for different retrieval tasks across trials, and Figure 1 shows that the ERPs associated with retrieval preparation differed according to the retrieval task. These differences were observed only on stay trials, where participants had completed the same retrieval task on the preceding trial, a finding consistent with the view that adopting fully a memory retrieval set takes at least one complete trial. 17 The pattern of differences across the types of preparatory cues is important, because as Figure 1 shows, there are commonalities and differences between the scalp distributions of the ERPs associated with the two preparatory episodic retrieval cues and the semantic preparatory cue 316
3 (which can be regarded as the baseline condition). Common to both preparatory episodic cues in comparison to the semantic cue is relatively greater activity at rightfrontal electrode locations, as indicated by the filled arrows at the top right as well as towards the foot of Figure 1. According to the logic outlined above, the shared differences between the preparatory episodic and semantic cues index retrieval mode, with the relatively greater positivity indicating that retrieval mode was engaged to an equivalently greater degree for the two episodic retrieval tasks relative to the semantic baseline task. At left fronto-central and at frontal-polar sites (see the unfilled arrows in Figure 1), the ERPs evoked by the two episodic preparatory cues diverge from each other. As described previously, the divergences between the ERPs evoked by the two episodic cues likely index the engagement of different retrieval orientations, presumably reflecting task-specific preparatory retrieval processing operations that are initiated according to the kind of episodic judgment that will be required when the subsequent test item is encountered. The distribution of the index of retrieval mode bears strong similarities with the distributions reported by other investigators who have demonstrated electrophysiological correlates of this class of retrieval process, 18,19 and is also broadly consistent with claims that right-prefrontal cortex is one brain region supporting retrieval mode. 20 The new information in these findings is that neural activity elicited by preparatory cues also varies according to the kind of episodic information that is to be retrieved. This validates the concept of retrieval orientation, and the distribution of the differences shown in Figure 1 is also consistent with the view that content specific retrieval processing operations are mediated by sub-regions of left pre-frontal as well as fronto-polar cortex (see 21,22 ). Retrieval Attempts Retrieval mode and orientation ensure that stimuli are treated as retrieval cues. 8,12,14 This implies that the successful adoption of these retrieval sets influences the processes set in train when a retrieval cue is encountered a retrieval attempt. The challenge for isolating neural correlates of retrieval attempts is to distinguish neural activity forming part of a retrieval attempt from activity indexing successful retrieval. One solution is to employ tasks requiring recovery of different episodic information. If those different tasks also involve a requirement to distinguish between new (unstudied) and old test items, then it is possible to contrast the activity elicited by new items separated according to retrieval task. 15,23-25 Since this class of retrieval cues has no study history in the experiment, any differences between the patterns of electrical activity elicited by them are potential correlates of a retrieval attempt. The same conclusion could not be drawn, however, on the basis of differences between the ERPs evoked by old (previously studied) items across tasks, because these differences may also reflect successful retrieval of different kinds of information in the two cases. 8 In several recent studies, ERPs evoked by new items have varied according to retrieval demands, and these differences are not simply a reflection of reaction time or of difficulty changes across tasks. 15,24,26-28 These indices of retrieval attempts can be conceived of as the consequences of having adopted successfully a retrieval orientation; that is, they are item-specific indices of retrieval orientation. Empirical support for this view stems from the fact that, in keeping with the finding that preparatory cue-related indices of orientation were reliable on stay trials only as already described (see 16 ), item-related indices of retrieval orientation are more pronounced in tasks where few rather than many switches between retrieval tasks are required. 29 In one recent illustrative study, Dzulkifli and Wilding 30 acquired ERPs during two retrieval tasks having different demands. Participants initially completed one of two encoding tasks on a series of visually presented words (all concrete nouns). For half of the words, participants had to think of and say aloud at least one use to which the object denoted by each word could be put. For the remainder, they had to rank on a 5-point scale how difficult the object denoted by each word would be to draw. In subsequent retrieval phases, words from one task were denoted as targets, and words from the other were denoted as non-targets. Participants had to make one response to targets, and another response to non-targets as well as to new test items. Across retrieval phases for each participant, words from either the function or the drawing tasks were denoted as targets. Figure 2 shows the ERPs evoked by new items, separated according to target designation. There are reliable differences between the neural activities elicited in the two conditions, primarily at frontal and central sites, which implies that the way participants interrogated their memories varied according to the instructions that were given. The likelihoods of correct judgments to targets and non-targets were >.80 and statistically equivalent in both target designations. Reaction times as well as the likelihoods of correct responses to new items also did not vary with target designation. This is important because it means that differences in task difficulty or response time are unlikely to explain the divergences between the ERPs evoked by the two classes of new items. 28 In light of these considerations, Dzulkifli and Wilding 30 interpreted these divergences as item-related indices of the engagement of different retrieval orientations. The ways in which these two classes of ERPs diverged is also of interest, because it does not correspond with disparities between ERPs evoked by classes of new items in other studies (cf. 26,28 ). According to the definition of orientation the processes engaged should vary according to task, and thus differences between the correlates of orientation 317
4 Figure 2. Grand average ERPs evoked by new words in the two target designation conditions. The data are shown for nine locations at midline as well as left- and right-hemisphere sites over anterior (F5, Fz, F6), central (C5, Cz, C6) and posterior scalp (P5, Pz, P6). The figure also shows scalp distributions for successive 100 ms time windows in which reliable differences between conditions were obtained. These distributions were computed from the scores obtained by subtracting mean amplitudes from the ERPs evoked by new words in the drawing target designation condition from those in the function condition. This is a modified version of a figure presented by Dzulkifli and Wilding. 30 should be observed across studies in which there have been different retrieval demands. Another notable aspect of the data in Figure 2 is that the relatively greater positivity for the ERPs from the function condition in comparison to the drawing condition is sustained for several hundred milliseconds. While the scalp maps in Figure 2 show that there is some change in the distribution of these ERP differences over time, there was no statistical support for this impression. The findings are therefore broadly consistent with the view that the same processes differentiate these two conditions over these time windows, a temporal pattern that has been observed in previous studies. 27,31 One explanation for this is that the differences between ERPs evoked by new items reflect for the most part the maintenance of task-dependent cue representations that are optimised to interact with appropriate memory traces. 13,26 These processes would of course be terminated around the time when the decision to make a new response to the test item is made. This is certainly not the only explanation for these ERP effects, however, and an alternative explanation is that the differences between ERPs elicited by classes of new items index processes that monitor for certain kinds of information that may be elicited by the interaction between a retrieval cue and a memory trace. 15 An important goal for future studies is a more precise characterization of what processes ensue from the successful adoption of a retrieval orientation than is available to date (see 24,31,32 ). Retrieval Success ERP Old/New Effects: As reviewed above, there is now a reasonable body of evidence indicating that ERPs evoked by new test items diverge in ways that are most parsimoniously interpreted as neural correlates of retrieval orientation. 33 In isolation, however, the findings due to Dzulkifli and Wilding 30 described above might seem a little counterintuitive. The reason for this is that one influential account of the way in which participants attempt to complete exclusion tasks is that they recollect information equally about targets as well as about non-targets. 34 If this assumption were correct, then assigning words from the function or drawing condition to the target category should make no difference to how people complete the tasks, because in both cases they would be attempting to recollect information about words from the drawing as well as from the function tasks. It follows from this supposition there would be little reason to anticipate differences between ERPs evoked by new items when words from either the function or drawing task are designated as targets. This is because stating that people approach the task in the same way irrespective of target designation is the same as saying that people are adopting the same retrieval orientation in the two cases. 318
5 Figure 3. Grand average ERPs evoked by correct judgments to targets, non-targets and new items acquired during the test phases of exclusion tasks. The data shown was acquired from a left-parietal (P5) electrode location. The data are collapsed across target designation and the figure is based on data presented in the study of Dzulkifli and Wilding. 30 Other aspects of the ERP data acquired during this task, however, offer a reasonable explanation for why evidence for the adoption of different orientations differences between ERPs evoked by new items and separated according to target designation should emerge. The critical data comes from analyses of ERP old/new effects, differences between the ERPs evoked by correctly identified old and new test items in memory retrieval tasks. 33 This contrast is the one to which most attention has been paid to date in ERP studies of memory retrieval. The logic behind this contrast is that differences between these two classes of stimuli reflect successful retrieval and/or its sequelae. 13 There is a family of ERP old/new effects, distinguishable on the basis of a combination of their time courses, scalp distributions and sensitivity to experimental variables. Space precludes a description of more than one effect here, although it is important to note that the presence of several electrophysiological indices of different retrieval processes has permitted ERPs to speak to a range of questions about the retrieval and post-retrieval processes that are compromised following medial temporal lobe damage, 35,36 in disease states, 37 during development, 38,39 and in healthy aging. 40 These indices have also been employed in order to distinguish between different cognitive accounts for various memory phenomena (for examples, see ). The ERP old/new effect we will focus on here is largest over parietal scalp and is evident primarily between 500 and 800 ms post-stimulus. It comprises a relatively greater positivity for correctly identified old than for correctly identified new test items. It is assumed to be an index of recollection, and the data that supports this view includes the following: 1. patients with deficits in recollection (as revealed by behavioral measures) exhibit attenuated or absent left-parietal ERP old/new effects relative to appropriately matched controls, 35-37,44 2. the magnitude of the effect is correlated positively with the amount of contextual information that is retrieved, as inferred from the numbers of correct source judgments that are made on retrieval tasks, 45 and 3. the effect is larger for correct old judgments associated with Remember (R) rather than with Know (K) judgments. 46 R judgments are held to be based upon recollection while K judgments are not. 47 While this data provides a compelling case for a link between the parietal old/new effect and recollection, some recent findings might be seen as counterintuitive, including those from the study of Dzulkifli and Wilding described above. 30 In that study, it was possible to analyse the leftparietal ERP old/new effects for correct judgments to targets as well as for non-targets, and one apparently reasonable assumption would be that the two old/new effects should be of relatively equal magnitude. This is based on the view that the way in which participants tackle this task is to attempt to recollect information about both study tasks (the function and the drawing tasks), and to make a target or non-target judgment when the appropriate information is recollected. In the study of Dzulkifli and Wilding, 30 however, the leftparietal old/new effect was markedly larger for targets than for non-targets, as Figure 3 shows. Given that this old/new effect is correlated with the amount of information recovered from episodic memory, 45 the ERP data suggest that participants prioritised successfully recovery of episodic information about targets over episodic information about non-targets. This pattern of data therefore explains the divergence between the ERPs evoked by new items in the function and drawing target designation conditions (see Figure 2), since the old/new effects are consistent with the view that participants adopted different retrieval orientations, the consequences of which were prioritisation of recollection of one form of mnemonic content in different target designation retrieval phases. Why might this prioritisation occur? The account for which there is now reasonable empirical support is that when the likelihood of recollecting information about targets is high, a strategy that will enable good performance on the task is to focus only on the recollection of information about targets, and to make a non-target judgment when recollection of target information fails. 27,48 The key observation that underlies this account is that in a task in which binary memory judgments are required (recall that new/non-target judgments are made on the same key), the 319
6 absence of information can be used as a basis for accurate judgments in some circumstances. This assumption is central to one influential account of how people decide on the source through which information was first acquired, 49 and these findings suggest that ERPs may be of some utility in testing the assumptions underlying this model. The fact that the left-parietal ERP old/new effect appears to be acting as an index of selective recovery of information from memory is also exciting for other reasons, since it provides a means of addressing a variety of questions concerning the control of memory retrieval. These include questions about: 1. the resolution with which memories with similar or dissimilar characteristics can be recovered selectively, 2. the brain regions that permit this selectivity, 3. the stages of memory retrieval at which this selectivity occurs, and 4. the mechanisms that support the selective control of recollection. The final point here is a particularly interesting avenue to explore, since one possibility is that selective recollection comes about as a result of active inhibitory processes that facilitate the recovery of some kinds of information at the expense of others. Failure to inhibit information that is not task-relevant is associated with frontal lobe deficits, increasing age and Alzheimer s disease. Thus this aspect of the electrical record may provide a means of linking memory deficits seen in certain populations with deficits in other cognitive domains. If nothing else, the findings to date certainly suggest that it would be fruitful to use this index of selective recollection as an assay for differences in the ability to retrieve selectively according to variables that would include site of brain damage, disease state, pharmacological manipulations and age. SUMMARY The purpose of this brief review was threefold. First, to sketch different stages of memory retrieval processing commonly assumed to contribute towards successful remembering. Second, to illustrate how ERPs can be and have been employed in conjunction with appropriate experimental designs in order to index memory retrieval processes that operate at these different stages. Third, to provide pointers to the ways in which these electrophysiological indices can be utilised in order to understand which memory retrieval processes are compromised in different populations. To date, ERP studies of episodic memory impairments have for the most part employed ERP old/new effects as the electrophysiological dependent variable (for one exception, see 50 ). The recent new insights offered by the ways in which the left-parietal ERP old/new effect might act as an index of selective memory retrieval means that there remains considerable mileage in this line of research. 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