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1246     D. L. Schacter & D. R. Addis      Constructiv...
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On the nature of medial temporal lobe contributions to the constructive simulation of future events (schacter & addis 2009)

  1. 1. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 On the nature of medial temporal lobe contributions to the constructive simulation of future events Daniel L. Schacter and Donna Rose Addis Phil. Trans. R. Soc. B 2009 364, 1245-1253 doi: 10.1098/rstb.2008.0308 References This article cites 49 articles, 10 of which can be accessed free http://rstb.royalsocietypublishing.org/content/364/1521/1245.full.html#ref-list-1 Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;364/1521/1245 Subject collections Articles on similar topics can be found in the following collections neuroscience (226 articles) Email alerting service Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2009 The Royal Society
  2. 2. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 Phil. Trans. R. Soc. B (2009) 364, 1245–1253 doi:10.1098/rstb.2008.0308 On the nature of medial temporal lobe contributions to the constructive simulation of future events Daniel L. Schacter1,2,* and Donna Rose Addis3 1 Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA 2 Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA 02129, USA 3 Department of Psychology, University of Auckland, Auckland 1142, New Zealand A rapidly growing number of studies indicate that imagining or simulating possible future events depends on much of the same neural machinery as does remembering past events. One especially striking finding is that the medial temporal lobe (MTL), which has long been linked to memory function, appears to be similarly engaged during future event simulation. This paper focuses on the role of two MTL regions—the hippocampus and parahippocampal cortex—in thinking about the future and building mental simulations. Keywords: memory; mental simulation; future thinking; hippocampus; medial temporal lobe; parahippocampal cortex 1. INTRODUCTION there were also strong commonalities between remem- Everyday experience suggests that predictions are bering the past and imagining the future. Positive past about the future, whereas memory is about the past. and future events were rated as more strongly experi- From this perspective, the two phenomena run on enced than negative past and future events, temporally parallel tracks in opposite temporal directions. For close events in either the past or future were more example, predictions about the future occur at varying strongly experienced and included more sensory and different time scales, ranging from situations where one contextual details than did distant events, and partici- enters a new setting, such as a school or a museum, and pants were more likely to adopt a first-person than third- tries to predict what might happen next (e.g. Bar person perspective for temporally close than temporally 2007), all the way to predicting how happy one might distant events in both the past and the future. be years or decades in the future in a marriage or a job These commonalities in cognitive processes under- (Gilbert 2006). Analogously, memory can operate on lying past and future events are complemented by the very recent past, as when we use working memory analogous similarities in brain activity: the same ‘core to recall the last few words in a sentence, or the remote network’ of brain regions is recruited when people past, as when we recall our childhood experiences. remember the past and imagine the future, including It is becoming increasingly clear, however, that medial prefrontal and frontopolar cortex, medial predicting the future and remembering the past may be temporal lobe (MTL), lateral temporal and tempor- more closely related than everyday experience might opolar cortex, medial parietal cortex including pos- suggest. For example, errors in predicting the future are terior cingulate and retrosplenial cortex, and lateral often based on how we remember the past (for a review, parietal cortex (for reviews, see Schacter et al. (2007, see Gilbert & Wilson 2007). In a related vein, 2008) and Buckner et al. (2008)). For memory remembering the past recruits many of the same cognitive researchers, perhaps the most striking finding from processes as does imagining or simulating the occurrence this research is that the MTL, a structure long known of possible events in the future. Consider, for example, to play a critical role in remembering, appears to be a study by D’Argembeau & Van der Linden (2004), in similarly involved when individuals imagine or simulate which they asked subjects to either remember a specific events that might occur in their personal futures. event from their past or imagine a specific event that The purpose of the present paper is to review recent could plausibly happen to them in the future, and rate evidence from our laboratory and others that links various attributes of the event. Although remembered MTL activity to future event simulation, to consider past events were associated with more vivid sensory and alternative interpretations of these observations, and to contextual details than were imagined future events, discuss them in relation to other evidence concerning the MTL and constructive memory. Elsewhere, we have provided broad reviews concerning cognitive and * Author and address for correspondence: Department of Psychol- ogy, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, neural aspects of future event simulation (Schacter et al. USA (dls@wjh.harvard.edu). 2007, 2008), and focus here instead on the contri- One contribution of 18 to a Theme Issue ‘Predictions in the brain: butions of two regions within the MTL, the hippo- using our past to prepare for the future’. campus and parahippocampal cortex. 1245 This journal is q 2009 The Royal Society
  3. 3. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 1246 D. L. Schacter & D. R. Addis Constructive simulation of future events 2. REMEMBERING THE PAST AND IMAGINING years), or the near or distant future (the next few days THE FUTURE: CONCEPTUAL ISSUES AND or years). These critical conditions were compared with THE CONSTRUCTIVE EPISODIC a semantic control task involving analysis of the SIMULATION HYPOTHESIS meaning of words. Compared with the control When we use such terms as ‘episodic simulation’ or condition, significant levels of activation were observed ‘future event simulation’, we refer to imaginative during both the past and future conditions in the right constructions of hypothetical events or scenarios that might hippocampus and bilateral parahippocampal cortex. occur in one’s personal future (Schacter et al. 2008). Furthermore, two left parahippocampal areas showed Although we focus on the idea that simulation is critical greater activity when individuals were thinking about for envisaging possible future events, we do not restrict the future than about the past. Moreover, activity in a our application of simulation to the future. People also number of these MTL regions was modulated by engage in simulations of present and past events, temporal distance. Most of them showed the same a point that will be important to consider in relation to neural response to temporal distance for both the past recent empirical observations and theoretical accounts. and future events: either increasing or decreasing Motivated in part by some of the striking common- activity with increasing temporal distance. The only alities noted earlier between remembering past events region that exhibited an interaction between temporal and simulating future ones, we advanced the constructive direction (i.e. past versus future) and distance (i.e. near episodic simulation hypothesis (Schacter & Addis versus distant) was an inferior region in the left 2007a,b; for related views, see Suddendorf & Corballis parahippocampus gyrus (BA 36), one of the two areas 1997, 2007; Buckner & Carroll 2007; Hassabis & noted above that showed greater activity for future than Maguire 2007). By this view, past and future events past events. In this region, Okuda et al. noted that the draw on similar information stored in episodic memory increase in brain activity from the near to distant future and rely on similar underlying processes: episodic tasks was smaller than the increase in activity observed memory supports the construction of future events by from the near to distant past tasks. extracting and recombining stored information into a These observations are potentially important simulation of a novel event. Indeed, we have suggested because they suggest that the parahippocampal and that simulation of future events requires a system that hippocampal regions are at least as active during future can flexibly recombine details from past events. event simulation as during remembering of past Taking an adaptive perspective, we (Schacter & experiences. Note, however, that because Okuda et al. Addis 2007a,b) suggested that a critical function of a used a relatively unconstrained paradigm that did not constructive memory is to make information available probe participants about particular events, it is unclear for simulation of future events. Episodic memory thus whether these reports consisted of episodic memories/ supports the construction of future events by flexibly simulations (unique events specific in time and place), recombining stored information into a simulation of a or general semantic information about an individual’s novel event. The adaptive value of such a system is that past or future. More recent functional magnetic it enables past information to be used flexibly in resonance imaging (fMRI) studies have used event- simulating alternative future scenarios without enga- related designs to yield information regarding the ging in actual behaviour. A potential downside of such neural bases of specific past and future events. a system is that it is vulnerable to memory errors, such Addis et al. (2007) used event-related fMRI to as misattribution and false recognition (e.g. Schacter & distinguish between an initial construction phase, where Addis 2007a,b; see also Suddendorf & Corballis 1997; participants generated a specific past or future event in Dudai & Carruthers 2005). response to an event cue (e.g. ‘dress’), making a button With respect to the MTL, it has been suggested that press when they had an event in mind, and an the hippocampal region supports relational memory elaboration phase during which participants generated processes that link together disparate bits of infor- as much detail as possible about the event. We mation (e.g. Eichenbaum & Cohen 2001). According compared activity during the past and future tasks to the constructive episodic simulation hypothesis, with control tasks that required semantic and imagery these processes are crucial for recombining stored processing, respectively. information into future event simulations. Thus, our We observed evidence of past- and future-related hypothesis posits an important link between hippo- MTL activities during both the construction and campal activity and the simulation of future events. elaboration phases. The construction phase was associated with common past–future activity in the posterior left hippocampus, which we suggested might 3. NEUROIMAGING OF PAST AND reflect the initial interaction between cues and hippo- FUTURE EVENTS campally mediated pointers to memory traces. Simi- A large number of neuroimaging studies have larly, the elaboration phase revealed evidence of examined brain activity when people remember past common past–future activity in the left hippocampus, autobiographical experiences (for reviews, see Svoboda possibly reflecting the retrieval and/or integration of et al. (2006) and Cabeza & St Jacques (2007)). additional event details into the memorial or imaginal By contrast, only a handful of studies have explored representations, as well as common past–future activity brain activity when people imagine future events. in the bilateral parahippocampal cortex. There was also Okuda et al. (2003) reported the first such study. evidence for differential engagement of MTL activity in During scanning, participants talked freely for 60 s the future task: during the construction phase, a region about either the near or distant past (last few days or of the right hippocampus showed increased activity Phil. Trans. R. Soc. B (2009)
  4. 4. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 Constructive simulation of future events D. L. Schacter & D. R. Addis 1247 only in the future condition. We suggested that this differentially to the amount of detail comprising future future-specific hippocampal activity might reflect the events, possibly reflecting the recombination of details novelty of future events and/or additional relational into a novel future event. processing required when one must recombine dis- The parametric modulation analysis of temporal parate details into a coherent event. distance revealed that the increasing recency of past Botzung et al. (2008) reported fMRI data that events was associated with activity in the right contrast with the aforementioned results showing parahippocampus gyrus (BA 35/36), while activity in increased hippocampal activity for future versus past the bilateral hippocampus was associated with the events. One day prior to scanning, subjects described increasing remoteness of future events. We proposed 20 past events from the last week and 20 future events that the hippocampal response to the distance of future planned for the next week. The subjects constructed events reflects the increasing disparateness of details cue words for these events that were then presented to probably included in remote future events, and the them the next day during scanning, when they were intensive relational processing required for integrating instructed to think of past or future events to each cue. such details into a coherent episodic simulation of Although past and future events produced activation in the future. Overall, these results suggest that, although a similar network to that reported by Okuda et al. MTL regions supporting past and future event (2003) and Addis et al. (2007), including bilateral simulation show impressive commonalities during MTL, Botzung et al. reported no evidence for increased event elaboration, they can be recruited in different activity in the future condition compared with the past ways depending on whether the generated event is in condition. In fact, they noted that both the right and the past or future. left hippocampus showed greater activity in the past A study by Addis et al. (2008a) provides additional condition than in the future condition. insight into the nature of MTL activity during the As we have pointed out elsewhere (Schacter et al. construction phase. Participants were cued to either 2008), however, participants in the Botzung et al. remember specific past events or imagine specific future (2008) study initially carried out their simulations of events, as in Addis et al. (2007). In addition, they were future events in a separate session prior to scanning, also cued to remember general routine events (e.g. having they thus may have recalled their prior simulation brunch after attending church) or to imagine generic during scanning, rather than constructing it for the first events that might occur in their personal futures (e.g. time, as subjects did in the earlier studies. Although reading the newspaper each morning). We reasoned that Botzung et al. excluded those trials in which subjects in a region that is responsive to the amount of detail stated that they produced an event from the pre-scan recombined into a coherent imagined episode, as we interview, it is unclear how reliably subjects can make suggested with respect to the hippocampus (Addis & the requested discrimination. Moreover, since subjects Schacter 2008), more activity should be evident when had previously encoded their future event simulation, constructing specific future events relative to general rather than constructing it anew during scanning as in future events (as well as specific and generic past events). previous studies, there may have been less recruitment By contrast, if the hippocampal region is simply of processes involved in recombining details from past responsive to the prospective nature of future events, experiences. Similar findings have been reported in then it should be more engaged during the construction other studies examining the retrieval of previously of both types of future events relative to past events, constructed imaginary events (Hassabis et al. 2007a; irrespective of specificity. D’Argembeau et al. 2008). We replicated the aforementioned findings of Two more recent studies from our laboratory have equivalent left hippocampal activity during the con- further examined the nature of hippocampal acti- struction of past and future events, and greater right vations observed during the construction and elabor- hippocampal activity for future than past event ation stages of event remembering and simulation, construction. Importantly, though, the increased right respectively. Addis & Schacter (2008) further analysed hippocampal activity was evident only for specific the elaboration-stage data reported initially by Addis events; in fact, there was no evidence for right et al. (2007), using parametric modulation analyses to hippocampal activity during construction of generic examine MTL activity according to the amount of future events. Thus, the results appear to provide detail generated and the temporal distance of each evidence against the idea that right hippocampal event from the present. We suggested that reintegrating activation for specific future events indicates a uniquely increasing amounts of detail for either a past or future prospective function for this region. Importantly, there event would be associated with increasing levels of were regions that did show activation patterns that hippocampal activity. However, future events should could be interpreted as reflecting as a prospective require more intensive recombining of disparate details function, such as the left frontopolar cortex, in into a coherent event, so the hippocampal response to which construction of future events resulted in greater increasing amounts of future event detail should be activity than past events, irrespective of the specificity larger than that for past event detail. Consistent with of the event. these predictions, the analysis showed that the left An event-related fMRI study by Hassabis et al. posterior hippocampus was responsive to the amount (2007a) also provides data that call into question the of detail for both the past and future events, probably idea that MTL activation during event simulation is reflecting the retrieval of details from episodic memory tied specifically to thinking about events in one’s future. that is required for both tasks. By contrast, a distinct Participants were asked to imagine novel, fictitious region in the left anterior hippocampus responded scenes, without explicit reference to whether those Phil. Trans. R. Soc. B (2009)
  5. 5. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 1248 D. L. Schacter & D. R. Addis Constructive simulation of future events scenes should be placed in the past, present or future. finding that the hippocampus was robustly activated Subjects were then scanned in a subsequent session in during event simulation when we experimentally which they were cued to remember the previously recombined details concerning person, object and place constructed fictitious scenes, construct additional from different episodes provides evidence against this novel fictitious scenes or recall real episodic memories recasting hypothesis. Although we would not rule out the from their personal pasts. Hassabis et al. found that possibility that recasting occurs on some test trials, all three conditions were associated with activations the finding of hippocampal activation in this paradigm, in the hippocampus, parahippocampal gyrus and which should minimize or eliminate recasting, is several other regions in the core network. The results consistent with the claim from the constructive episodic thus indicate that activity in these regions is not simulation hypothesis, that activity in the hippocampus restricted to conditions that explicitly require imagin- during event simulation reflects the recombination of ing future events. details from different episodes. Additional evidence on this point is provided by One feature common to the neuroimaging studies another recent study from our laboratory. Addis et al. reviewed so far is that each one provided some evidence (in press) approached the question of whether future for activity in both the hippocampal and parahippo- event-related activity is specifically associated with campal regions in conditions designed to elicit future prospective thinking, or with the more general event simulation (Okuda et al. 2003; Addis et al. 2007, demands of imagining an episodic event in either in press; Botzung et al. 2008) or imagination (Hassabis temporal direction, by instructing subjects to imagine et al. 2007a). Szpunar et al. (2007) reported a events that might occur in their personal future or contrasting pattern of results. In their fMRI study, events that might have occurred in their personal participants were given event cues, such as past birthday pasts but did not. Prior to scanning, participants or retirement party, and were instructed to remember provided episodic memories of actual experiences specific events from their personal pasts, imagine that included details about a person, object and place specific events that might reasonably occur in their involved in that event. During scanning, the subjects personal futures or imagine specific events that could were cued to recall some of the events that had involve a familiar individual (Bill Clinton). Compared actually occurred, and for the conditions in which with the latter condition, remembering one’s personal they imagined events, the experimenters randomly past or simulating one’s personal future was associated recombined details concerning person, object and with significant and comparable levels of activity in the place from separate episodes. Participants were thus bilateral parahippocampal cortex, as well as other presented with cues for a person, object and place regions activated in other studies, including other taken from multiple episodes, and were instructed to posterior regions such as posterior cingulate and imagine a single, novel episode that included the anterior regions such as the frontopolar cortex. By specified details. contrast, no evidence for hippocampal activation was With respect to the MTL, Addis et al. (in press) reported in the personal past or future conditions reported that both the hippocampus and parahippo- relative to the ‘Bill Clinton’ control. We will return to campal cortex were similarly engaged when partici- pants imagined future and past events, suggesting this observation later when considering theoretical that these regions (as well as others in the core network implications of the aforementioned results. that showed the same pattern) can be used for Szpunar et al. (in press) sought to characterize the event simulation regardless of the temporal location nature of activity they had observed in the para- of the event. hippocampal and related posterior regions. They This study also allowed us to address an issue that is noted previous work from Bar & Aminoff (2003), particularly relevant to the constructive episodic suggesting that the parahippocampal cortex and simulation hypothesis discussed earlier, which empha- posterior cingulate are involved in processing con- sizes that future event simulations are built by flexibly textual associations, thus suggesting that these recombining details from past experiences, probably regions may be responsible for generating the familiar engaging the relational processes supported by the contexts in which future event simulations are hippocampus. However, our previous studies on situated (Addis et al. 2007; Szpunar et al. 2007). To imagining future events did not provide direct evidence test the idea, Szpunar et al. asked participants to that subjects recombine details from multiple past imagine themselves in future scenarios involving events into novel future simulations. An alternative either a familiar or an unfamiliar context; they also possibility is that participants simply recast their asked participants to remember past experiences memories of individual past experiences as imagined involving familiar contexts. They carried out region- future events, especially when they are thinking about of-interest analyses focused on the areas within the events that might plausibly occur in the near future. For bilateral parahippocampal cortex and posterior example, when given the cue ‘car’ and asked to imagine cingulate that had been activated in their previous an event that might occur in the next few weeks study. Consistent with the hypothesis that these involving a car, participants might simply recall a recent regions are important for instantiating contextual episode in which they saw a car cross a red light, and information, both regions showed robust activity in imagine that such an incident might occur in the next the past and future conditions that required gener- few weeks. When this kind of recasting process occurs, ating a familiar context, and significantly less activity there is little or no recombination of details of past in the future condition that required generating an events into imagined future scenarios. However, the unfamiliar context. Phil. Trans. R. Soc. B (2009)
  6. 6. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 Constructive simulation of future events D. L. Schacter & D. R. Addis 1249 4. STUDIES OF AMNESIC PATIENTS AND known to be dependent on the hippocampus. Second, OLDER ADULTS hippocampal atrophy has been documented in older Although most of the evidence linking future event adults (e.g. Driscoll et al. 2003). simulation with MTL activity comes from neuroima- ging studies, additional evidence is provided by studies of amnesic patients, who exhibit an impairment in the 5. MTL AND FUTURE EVENT SIMULATION: ability to remember past experiences as a result of SUMMARY, EXTENSIONS AND THEORETICAL bilateral damage to the MTLs and related structures. IMPLICATIONS Tulving (1985) reported that the severely amnesic The studies reviewed in the preceding sections are patient K. C., who cannot remember any specific broadly consistent with the idea that regions within the episodes from his past (for a review of K. C., see MTL are associated with constructing simulations of Rosenbaum et al. 2005), exhibits similar problems future events. We discuss now a number of points envisioning any specific episodes in his future. K. C. is regarding these studies and related research that has characterized by bilateral MTL damage, but also has characterized MTL function in different domains. extensive prefrontal damage, and in other regions (see First, consider the neuroimaging studies that we Rosenbaum et al. 2005), so it is unclear whether his reviewed. On balance, the most consistent feature of problems imagining the future are associated speci- the neuroimaging data is that both the hippocampus fically with the MTL. A similar caveat applies to a more and parahippocampal cortices are similarly active recent study concerning patient D. B., who became during the simulation of future events and the amnesic as a result of cardiac arrest and consequent remembering of past events, in agreement with a anoxia (Klein et al. 2002). D. B. showed clear deficits meta-analysis by Spreng et al. (in press). In addition, on a 10-item questionnaire probing past and future however, it is clear that this common activation of the personal events that were matched for temporal hippocampus and parahippocampus is not restricted to distance from the present. However, even though conditions requiring prospective event simulation: the anoxia is typically associated with MTL damage, no same regions are engaged when individuals are neuroanatomical findings were reported concerning instructed to simulate events that might have occurred patient D. B. in their pasts (Addis et al. in press) or when asked to Hassabis et al. (2007b) examined the ability of five imagine scenes without a specific temporal reference patients with documented bilateral hippocampal amne- (Hassabis et al. 2007a). This latter finding fits well with sia to imagine novel experiences, such as ‘imagine the related observations that both regions show you’re lying on a white sandy beach in a beautiful similarly increased activity during tasks involving tropical bay’. The experimenters scored the construc- spatial navigation (for a review, see Buckner & Carroll tions of patients and controls based on the content, 2007; Spreng et al. in press) and, under some spatial coherence and subjective qualities of the conditions, during tasks requiring theory of mind imagined scenarios. Four of the five hippocampal judgements, which commonly activate medial pre- patients produced constructions that were significantly frontal and parietal regions of the core network reduced in richness and content, and especially, the (Buckner & Carroll 2007; Spreng et al. in press; but spatial coherence of the scenarios, relative to scenarios these structures are probably not necessary for some constructed by controls. The single patient who theory of mind tasks on which amnesic patients performed normally on the imaginary scene task perform well; see Rosenbaum et al. 2007). maintained some residual hippocampal tissue. Since Even though more evidence is required given the the lesions in the other cases appear to be restricted to relatively small database, in general, extant results hippocampal formation, this study strengthens the link support the view that the hippocampal and parahippo- between event simulation and hippocampal function. campal regions are engaged when individuals build We also note that a recent study by Addis et al. simulations of events located in the future, past or (2008b) provides evidence that future event simulation present. Thus, although our focus in the present paper is impaired in older adults, who also exhibit memory remains on the simulation of future events, it seems impairments, albeit considerably milder than those likely that ideas concerning the role of MTL regions seen in amnesic patients. Young and older participants apply more broadly to other kinds of simulations. generated memories of past events and simulations of Another issue raised by neuroimaging studies future events in response to individual word cues, and concerns the evidence that the hippocampal and transcriptions of the events were segmented into parahippocampal regions can be differentially engaged distinct details that were classified as either internal by tasks requiring future event simulation compared (episodic) or external (semantic; cf. Levine et al. 2002). with autobiographical remembering. Addis et al. The key finding was that older adults generated fewer (2007) reported that the right hippocampus shows internal (but not external) details than younger adults; greater activity during construction of future than past importantly, this effect was observed to the same extent events, a finding that we subsequently replicated when for future events as for past events. Although there is no demonstrating that the effect occurs for specific but not direct evidence from this study linking the age-related general future events. By contrast, Okuda et al. (2003) deficits to MTL dysfunction, two kinds of indirect reported greater future than past activity for two areas evidence suggest that such a link may exist. First, we within the left parahippocampal gyrus. The contrasting reported that the internal (but not external) detail score results suggest that interpretive caution must be in older adults correlated significantly with a measure exercised regarding a possible difference between the of relational memory (paired-associate learning) that is hippocampal and parahippocampal regions in this Phil. Trans. R. Soc. B (2009)
  7. 7. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 1250 D. L. Schacter & D. R. Addis Constructive simulation of future events respect, but given that the right hippocampal effect has By contrast, a region of the left posterior hippocampus been replicated, and the methodological concerns ( yZ30) was engaged by all tasks requiring the retrieval noted earlier regarding the Okuda et al. (2003) of relational information (i.e. correct recognition of study, we are inclined to assign more weight at the A–B, B–C and A–C pairs). Linking these observations present time to the hippocampal than the parahippo- with the aforementioned data from Addis & Schacter campal finding. (2008), perhaps both the past and future events require We have suggested that the future greater than past the retrieval of some form of relational information (i.e. activity in the right hippocampus could reflect the more details that were encoded as part of a complex intensive constructive activity associated with recom- autobiographical memory) and commonly engage the bining details of past events to generate a novel future posterior hippocampus, whereas only future events event (Addis et al. 2007). Note that this effect require recombining such details, and thus, as in was observed in the right anterior hippocampus Preston et al.’s study, recruit the anterior hippocampus. (Talairach xyz coordinateZ40, K22, K11 for the The foregoing observations might be useful in peak voxel in Addis et al. (2007)). This idea fits thinking about one of the puzzling findings from nicely with our thinking about the finding reported by neuroimaging research noted earlier: in contrast to Addis & Schacter (2008) during event elaboration, other studies, Szpunar et al. (2007) did not report where activity in a left anterior hippocampal region evidence of hippocampal activation when individuals (xyzZK20, K22, K6) correlated with the amount of simulated events in their personal futures, compared detail in future but not past events, while left posterior with when they imagined Bill Clinton participating in hippocampal activity (xyzZK18, K34, 1) correlated similar kinds of events. We suggested that both of these with both the future and past details. This latter region tasks probably involve the kind of relational processing is quite close to the posterior hippocampal region and recombining of event details thought to elicit associated with the amount of retrieved detail in an hippocampal activation. If so, significant hippocampal earlier study of autobiographical memory (xyzZK20, activation during each task would not be evident in a K37, 0; Addis et al. 2004). These observations led us to comparison between tasks. propose that the anterior hippocampal region is Of course, the question of whether hippocampal specifically involved in recombining details from past regions are necessary for simulating future events events, converging with our account of the future cannot be answered by neuroimaging studies alone, greater than past activity during construction in the which are necessarily correlational in nature. More- right anterior hippocampus. over, the imaging evidence leaves open the question of These ideas also fit with findings from other memory whether hippocampal activity during future event paradigms. In a meta-analysis of MTL activations simulation reflects retrieval and /or recombination of during encoding and retrieval, Schacter & Wagner event details, as we have suggested, versus the (1999) noted evidence linking anterior hippocampal encoding and storage of novel information. As we activity with relational or associative processing at both have stressed, future event simulations involve the encoding and retrieval. Subsequent research has been construction of novel scenarios, and the hippocampus largely consistent with this observation, as anterior regions of the hippocampus showed preferential appears to play a role in the encoding of novel activation in conditions requiring relational processing events (e.g. Ranganath & Rainer 2003). Evidence at both encoding (e.g. Giovanello et al. 2004; Jackson & reviewed earlier indicating impaired future event Schacter 2004; Kirwan & Stark 2004; Chua et al. 2007) simulation in amnesic patients is consistent with the and retrieval (Giovanello et al. 2004; Kirwan & Stark idea that the hippocampal region is indeed necessary 2004). Recent work using functional connectivity for retrieving and /or recombining event details into a analyses of rest fMRI data has suggested that the representation that supports simulation of the future, anterior and posterior hippocampus are connected but further studies of amnesic patients are required to with distinct cortical systems (Kahn et al. 2008). understand more fully the nature and extent of their Findings reported by Preston et al. (2004; see also simulation deficits. Heckers et al. 2004) point towards an even further Intriguingly, several recent studies of rodents have possible refinement of the foregoing ideas, suggesting shown that hippocampal neurons code for prospective that left anterior hippocampal activity ( yZK22) is information concerning where the rat needs to go in the associated specifically with recombining elements from immediate future (e.g. Ferbinteanu & Shapiro 2003; previously learned associations. They used a transitive Foster & Wilson 2007; Johnson & Redish 2007). For inference design in which participants first learned to instance, Johnson & Redish (2007) recorded from associate specific faces (stimuli A) with specific houses ensembles of neurons with place fields in the CA3 (stimuli B), and then learned to associate another set of region of the hippocampus, allowing them to analyse faces (stimuli C) with the same houses (stimuli B). activity during choices made by rats in a spatial decision Critically, the A and C faces were not shown together task. On some trials, the spatial representation during training, but were related to one another reconstructed from the neural ensemble appeared to through their overlapping associations with the same indicate possible future paths, leading Johnson and house (B). During scanning, correctly recognizing that Redish to suggest that the hippocampus may be a the A–C face pair contained related elements signi- source of prospective memory signals. It will be ficantly engaged the left anterior hippocampus relative important to investigate whether and to what extent to all other recognition conditions, including successful such findings are related to the observations on future recognition of A–B and B–C face–house pairs as ‘old’. event simulation in humans considered here. Phil. Trans. R. Soc. B (2009)
  8. 8. Downloaded from rstb.royalsocietypublishing.org on 6 October 2009 Constructive simulation of future events D. L. Schacter & D. R. Addis 1251 Let us also consider the role of the parahippocampal events, so it would make sense from the perspective of region in future event simulation. As we have seen, this the reality monitoring framework that regions associ- region is activated consistently in neuroimaging studies ated with processing of sensory and contextual details as part of a more general core network. Although would show greater activity for real than imagined hippocampal and parahippocampal regions generally events. show similar activity patterns, there are reasons to posit Although much work remains to be done, we believe that they play different roles within the network. that the research considered here has the potential to Evidence discussed earlier from Szpunar et al. enrich, broaden and, perhaps, alter our ideas about the (in press) suggests that the parahippocampal region nature and functions of memory, as well as our thinking (along with posterior cingulate) is important for about how the MTL allows us to stay connected with generating familiar contexts that contribute to future both the past and the future. event simulations. This idea fits well with the previously mentioned studies of Bar & Aminoff (2003; see also, The preparation of this paper was supported by grants from Bar 2007), which have independently implicated the the NIMH and NIA. 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