Elsevier

Neuropsychologia

Volume 47, Issue 11, September 2009, Pages 2261-2271
Neuropsychologia

Ventrolateral prefrontal cortex and self-initiated semantic elaboration during memory retrieval

https://doi.org/10.1016/j.neuropsychologia.2008.10.024Get rights and content

Abstract

Left ventrolateral prefrontal cortex (LVPFC) is often implicated in neuroimaging studies of context memory retrieval. This activation has been argued to reflect proactive semantic processing that facilitates recollection of past events, or instead to reflect a reactive response to experienced episodic interference. We investigated these characterizations in an fMRI study that manipulated the relative distinctiveness of encoding across subsequent targets and lures by varying encoding task manipulations. Critically, during later testing, retrieval queries and prior target processing where held constant across the distinctive and non-distinctive testing conditions, and therefore any differences in cortical activity would be linked to subject-initiated retrieval strategies. We found that LVPFC activity was specific to context retrieval under distinctive conditions even though this condition demonstrated the least interference. The results suggest that this region is critical for self-initiated semantic elaboration during retrieval, and this conclusion was bolstered by finding that LVPFC activity predicted individual differences in context memory discrimination. In line with Tulving's Encoding Specificity Principle, we suggest that subjects actively construct semantic retrieval cues, reflected in increased VLPFC activation, in an attempt to isolate the distinctive semantic features of hypothetical experiences when possible. If successful, this improves the match between retrieval cue and engram and facilitates performance.

Introduction

Left ventrolateral prefrontal cortex (LVPFC; BA 45/47) activation has been observed during semantic processing, particularly when semantic judgments are loosely constrained and non-automatic (Badre & Wagner, 2002; Cabeza & Nyberg, 2000; Gold & Buckner, 2002; Petersen, Fox, Posner, Mintun, & Raichle, 1988; Poldrack & Wagner, 2004; Thompson-Schill, 2003; Wagner, Paré-Blagoev, Clark, & Poldrack, 2001). A less appreciated regularity is the finding of LVPFC activity across a range of episodic retrieval judgments (Buckner, 1996; Buckner & Wheeler, 2001; Lepage, Ghaffar, Nyberg, & Tulving, 2000; Tulving, Kapur, Craik, Moscovitch, & Houle, 1994). Notably, activation has been reported in a variety of context memory tasks, in which participants attempt to retrieve specific episodic details regarding prior stimulus encounters, such as deciding if probe items were presented during a particular prior rating or decision task. In contrast, when memory judgments are based on item familiarity or novelty (e.g. determining if the item had simply been presented before regardless of context) minimal LVPFC activation is observed (Dobbins, Foley, Schacter, & Wagner, 2002, Dobbins, Rice, Wagner, & Schacter, 2003; Henson, Rugg, Shallice, Josephs, & Dolan, 1999; Nolde, Johnson, & Raye, 1998; Ranganath, Johnson, & D’Esposito, 2000; Rugg, Fletcher, Chua, & Dolan, 1999; Rugg, Henson, & Robb, 2003; Yonelinas, 2002). The increased recruitment of LVPFC during context relative to item memory has been interpreted as reflecting controlled semantic operations that facilitate the intentional recollection of specific details about a past event. Although some research has been devoted to understanding the role of LVPFC in cognitive control of contextual memory, the nature of its contribution remains unclear.

Recent studies have argued for a multi-process model of the LVPFC, proposing important functional distinctions within this region (Badre, Poldrack, Paré-Blagoev, Insler, & Wagner, 2005; Danker, Gunn, & Anderson, 2008; Dobbins & Wagner, 2005; Gold et al., 2006). Specifically, several research reports have suggested that anterior LVPFC (BA 47/45) is involved with the controlled retrieval of semantic information (Badre et al., 2005, Fiez, 1997, Poldrack et al., 1999, Wagner et al., 2001) whereas posterior LVPFC (BA 45/44) is perhaps more involved in the selection of task-relevant information amongst irrelevant competing representations, regardless of whether those representations are semantic, episodic, or phonological (Buckner, 2003, Moss et al., 2005; Thompson-Schill, D’Esposito, Aguirre, & Farah, 1997; Thompson-Schill, D’Esposito, & Kan, 1999; Thompson-Schill, Bedny, & Goldberg, 2005). Although conceptually similar, these controlled semantic retrieval and general selection hypotheses differ in important ways in terms of their characterizations of activation during episodic memory retrieval. More specifically, the general selection account suggests that activation reflects a reactive control mechanism used to overcome interference and conflict among episodic representations. The engagement of the selection process would occur transiently, rather than in a sustained fashion, only when irrelevant information to perform the task is accidentally retrieved (Braver, Gray, & Burgess, 2007; Snyder, Feigenson, & Thompson-Schill, 2007). This type of mechanism has also been termed a “back-end” monitoring strategy whereby subjects rely on post-retrieval selection or monitoring processes to resolve ambiguous retrieval outcomes (Velanova, Lustig, Jacoby, & Buckner, 2007).

In contrast, the controlled semantic retrieval hypothesis posits a top-down mechanism employed as subjects build descriptive retrieval cues to aid episodic retrieval in a goal-directed manner. These proactive processes are thought to play a key role in episodic remembering as they permit the retrieval or attentional foregrounding of semantic information that would have been highly relevant during hypothetical prior encounters. If successful, this elaborative process increases overlap between the semantic information being considered during the retrieval attempts, and that which would have been central had the probe actually been encountered. This in turn is expected to increase the odds of recollection in the case of positive memory probes and also to reduce the likelihood false endorsement for negative probes. The importance of the relationship between encoding and retrieval operations has remained central in episodic memory research since the landmark work of Tulving et al. demonstrating that recollection depends on the extent to which the information provided by the retrieval cues overlaps with that which was central during the encoding of prior experiences (Tulving, 1983; Tulving & Thomson, 1973). Tulving and colleagues termed the importance of this match the “Encoding Specificity Principle” (see also Morris, Bransford, & Franks, 1977; Weldon & Roediger, 1987). To quote Tulving (1983) “The engram of an event stored in the episodic system, and the retrieval cue, as interpreted or encoded in light of the information in the semantic system, must be compatible for remembering to occur” (italics added p. 224). Thus, from this perspective, the potential for success during episodic retrieval attempt critically relies upon the nature of the semantic processing that subjects engage in during retrieval attempt.

Herein, we refer to the semantic processing occurring during episodic retrieval attempt as “semantic elaboration” and assume that these semantic operations are similar to those that are often critical for the original encoding of episodes (e.g., Kahn, Davachi, & Wagner, 2004; Nyberg, Habib, McIntosh, & Tulving, 2000; Nyberg et al., 1996; Vaidya, Zhao, Desmond, & Gabrieli, 2002). A critical difference however between the semantic operations executed during encoding, and those that the Encoding Specificity Principle assumes critical during retrieval, is that the former are typically more heavily constrained or dictated by the encoding environment whereas the latter depend upon subject's inferences about the types of information likely central for the putative prior experiences, and their belief that considering this information may trigger recollection of the actual event.

Consistent with the view that anterior LVPFC aids semantic elaboration during retrieval is the finding that activation in this region during source memory tasks is present when the conceptual details of the probes are relevant to the possible prior source contexts (e.g. remembering having made a pleasant/nonpleasant versus a living/nonliving judgment at encoding for presented test items), but not when it was the prior perceptual features that were critical for the current memory judgment (e.g. whether the object had appeared in a large or small size at encoding; Dobbins & Wagner, 2005). Since this retrieval activation overlaps with that reported in semantic retrieval studies (Dobbins et al., 2002, Ranganath et al., 2000, Wagner et al., 1998), this suggests that that recruitment of this region depends on the nature of the to-be-recollected details, with subjects choosing to semantically process retrieval items only when the sought remembrances are linked to the semantic features of the probes. According to these findings, anterior VLPFC is critical during some contextual recollection tasks because it enables retrieval of semantic attributes of the probe items most closely related to the desired episodic information. Furthermore, subjects are assumed to flexibly weight different features of the probes during remembering, depending upon their belief about the information that is most diagnostic for identifying the origin of a memory (Dobbins, Kroll, Yonelinas, & Lui, 1998; Johnson, Hashtroudi, & Lindsay, 1993). Such proactive strategies enable the access and active maintenance of semantic featural information that is task-relevant and presumably require the subjects’ awareness that semantic analysis of the targets and lures should aid remembering (Braver et al., 2007, Wagner et al., 2001).

Although prior work suggests that LVPFC contributes to semantic elaboration during retrieval, characterizing this process as self-initiated or strategic is perhaps premature because the type of the to-be-remembered information has been usually fairly evident given the retrieval query alone. For example, in Dobbins et al. (2002) subjects were prompted to select the one of three retrieval probes previously encountered during a pleasant/unpleasant rating task using the prompt “Pleasant Item?”. Under these settings, although the processing can be characterized as semantic elaboration, it is not clear to what extent one would want to refer to it as strategic or self-initiated because the retrieval prompt itself clearly identifies what type of probe information is most relevant, namely, semantic features linked to item pleasantness. That is, to the extent the critical item features are made explicit by the retrieval cue or prompt, this minimizes any demand for the subjects to recruit elaborative strategies in a self-initiated fashion. Since it is generally accepted that self-initiation of control processes plays a key role in supporting memory (Bissig & Lustig, 2007; Braver et al., 2007; Craik & Byrd, 1982; Derwinger, Neely, & Bäckman, 2005; Kapur et al., 1996; Mäntylä & Nilsson, 1983; Velanova et al., 2007) this represents a notable potential shortcoming. For example, Kirchhoff and Buckner (2006) examined patterns of encoding activity when subjects were unconstrained intentional encoding instructions. The data demonstrated that individuals’ self-initiated use of various encoding strategies predicted later retrieval accuracy. Significantly, the engagement of verbal/semantic elaboration was associated with activation in a network of regions that included LVPFC, while perceptual inspection strategies elicited extrastriate activation (Kirchhoff & Buckner, 2006). Thus, evidence suggests that during episodic encoding, anterior regions of the LVPFC may contribute to self-initiated, proactive semantic elaboration processes at encoding. Interestingly, the tendency to self-initiate this strategy, at least during encoding, can be influenced by prior training (Derwinger et al., 2005; Bissig & Lustig, 2007). Studies targeting retrieval tasks in episodic memory have not yet tested if such self-initiated semantic elaboration predicts memory performance and how it correlates with PFC activation patterns.

Here we investigate semantic elaboration and general selection characterizations of the role of the LVPFC during retrieval, in an event-related fMRI study. During encoding subjects saw two sequential lists of words and performed either the same semantic rating task across the two lists (non-distinctive encoding) or different semantic tasks across the lists (distinctive encoding). This design enabled us to render the processing of the first list either distinctive, or non-distinctive with respect the second list (Fig. 1). During subsequent context retrieval, participants were presented with words from the previous encoding lists and new words and were asked to decide whether each presented word was from a particular list (Is this word from List 1?). Critically, in the non-distinctive condition, retrieval of the prior semantic tasks performed on the items poorly discriminated the list origins (because it was the same across lists) whereas during the distinctive case such memory content was predicted to be of substantial benefit. Because the retrieval prompt remained the same across distinctive and non-distinctive testing conditions (i.e., Is this word from List 1?), any differences in controlled processing between conditions should reflect subject-initiated changes in adopted retrieval strategies. We hypothesized that PFC regions critical for the self-initiated semantic elaboration of the probes, should demonstrate increased activity for the distinctive relative to the non-distinctive condition. In contrast, regions involved in general selection demands should demonstrate greater activation in the non-distinctive compared to the distinctive condition, given the greater difficulty in contextual responding due to the high similarity of the episodic representations.

Section snippets

Subjects

Eighteen English-speaking volunteers (18–31 years old, 12 females) were included in the study. Informed consent was obtained in a manner approved by the Institutional Review Board of Duke University Medical Center. Two volunteers were excluded from the analyses, given that their behavioral performance was at chance.

Materials

A total of 480 words were drawn randomly from a pool of 1216 words. From this set, six lists of 80 items were constructed for use in six study/test cycles. The items in the pool

Behavioral data

Fig. 2 illustrates the mean “yes” rates for the three item origins during the context and item memory tasks. During both tasks, “yes” responses to List 1 items are correct responses (empty boxes) and “yes” responses to new items are incorrect (solid boxes). However the tasks differ in terms of the correctness of “yes” responses to List 2 items. These responses are incorrect during the context task and reflect List 2 intrusion errors. During the item memory task these indicate correct

Discussion

The current study examined two different cognitive control hypotheses with respect to the role of LVPFC during episodic retrieval. Unlike prior studies looking at these issues, here the prior processing of target retrieval probes and the format of retrieval prompts were held constant across conditions that were predicted to differ in terms of recruitment of self-initiated semantic elaboration versus the need to select among competing episodic representations. More specifically, the semantic

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