Motivated Memories: Effects of Reward and Recollection in the Core Recollection Network and Beyond.

fMRI was employed to assess whether the neural correlates of accurate source memory are modulated by the reward value of recollected information. Study items comprised pictures of objects, each paired with a depiction of 1 of 2 coins. The reward value of the coins ($2.00 vs. $0.02) was disclosed after study. At test, a source memory procedure was employed in which subjects discriminated between studied and unstudied objects and, for objects judged studied, indicated the identity of the coin paired with the object at study. Correct judgments earned a reward corresponding to the value of the coin, whereas incorrect judgments were penalized. No regions were identified where the magnitude of recollection effects was modulated by reward. Exclusive effects of source accuracy were evident in the hippocampus. Different striatal sub-regions demonstrated exclusive recollection effects, exclusive reward effects, and overlap between the 2 effects. The left angular gyrus and medial prefrontal cortex were additively responsive to source accuracy and the reward. The findings suggest that reward value and recollection success are conjointly but independently represented in at least 2 cortical regions and that striatal retrieval success effects cannot be accounted for in terms of a single construct, such as goal satisfaction.

Temporal dissociations within the core recollection network.

We investigated whether time courses of fMRI BOLD activity in recollection-sensitive brain regions varied according to the time over which recollected information was maintained. Human subjects studied word-picture pairs and were subsequently tested with studied and unstudied pictures during a scanned test phase. The test requirement was to judge whether each picture was old or new and, if old, to retrieve its study associate and hold it in mind until a response cue appeared. The interval between the test item and cue varied between two and eight seconds. Separate responses were required when items were deemed new or the associate was not retrieved. Whereas recollection-related activity in the posterior cingulate, medial temporal, and medial prefrontal cortices was transient and unrelated to the maintenance interval, activity in the left anterior angular gyrus (aLAG) tracked the interval. Thus, as in a prior study, recollection-sensitive regions could be temporally dissociated.

Perirhinal-hippocampal connectivity during reactivation is a marker for object-based memory consolidation.

The present study utilized event-related fMRI to address the role of the human perirhinal cortex (PRC), and its interactions with the hippocampus, in memory consolidation. Participants encoded object-based and scene-based associations and then restudied them either after a "long" or "short" delay during which consolidation could occur. We found that BOLD activation in left PRC and hippocampal-PRC functional connectivity were significantly enhanced during the restudy of the long versus short delay word-object pairs. Secondly, hippocampal-PRC connectivity during restudy of the long delay word-object pairs predicted a subsequent reduction in associative forgetting. By contrast, hippocampal-PRC connectivity did not predict subsequent resistance to forgetting for the short delay or novel associations. Together, these results provide evidence for perirhinal-hippocampal interactions in the selective consolidation of object-based associative memories and provide support for the notion that, during early stages of consolidation, memories become more distributed across brain regions.

Brain networks underlying episodic memory retrieval.

The importance of the medial temporal lobe to episodic memory has been recognized for decades. Recent human fMRI findings have begun to delineate the functional roles of different MTL regions, most notably the hippocampus, for the retrieval of episodic memories. Importantly, these studies have also identified a network of cortical regions--each interconnected with the MTL--that are also consistently engaged during successful episodic retrieval. Along with the MTL these regions appear to constitute a content-independent network that acts in concert with cortical regions representing the contents of retrieval to support consciously accessible representations of prior experiences.

The neural correlates of recollection: transient versus sustained FMRI effects.

Prior research has identified several regions where neural activity is enhanced when recollection of episodic information is successful. Here, we investigated whether these regions dissociate according to whether recollection-related activity is transient or sustained across the time that recollected information must be maintained before a behavioral judgment. Human subjects studied a series of word-picture pairs under the requirement to judge which of the denoted objects was smaller. Following each of 4 study sessions, a scanned test phase occurred in which a series of studied and unstudied words was presented. The requirement at test was to judge whether each word was old or new and, if judged old, to retrieve the associated study picture and hold it in mind until a cue appeared. The delay interval varied between two and eight seconds. The cue instructed subjects which of three different judgments should be applied to the retrieved picture. Separate responses were required when words were either deemed new or the associated image was not retrieved. Relative to studied words for which the associated picture could not be retrieved, words giving rise to successful recollection elicited transient responses in the hippocampus/parahippocampal cortex and retrosplenial cortex, and to sustained activity in prefrontal cortex, the intraparietal sulcus, the left angular gyrus and the inferior temporal gyrus. The finding that recollection-related activity in the angular gyrus tracked the period over which recollected information was maintained is consistent with the proposal that this region contributes to the online representation of recollected information.

Item memory, context memory and the hippocampus: fMRI evidence.

Dual-process models of recognition memory distinguish between the retrieval of qualitative information about a prior event (recollection), and judgments of prior occurrence based on an acontextual sense of familiarity. fMRI studies investigating the neural correlates of memory encoding and retrieval conducted within the dual-process framework have frequently reported findings consistent with the view that the hippocampus selectively supports recollection, and has little or no role in familiarity-based recognition. An alternative interpretation of these findings has been proposed, however, in which it is argued that the hippocampus supports the encoding and retrieval of 'strong' memories, regardless of whether the memories are recollection- or familiarity-based. Here, we describe the findings of eight fMRI studies from our laboratory: one study of source memory encoding, four studies of the retrieval of contextual information, and three studies of continuous recognition. Together, the findings support the proposal that hippocampal activity co-varies with the amount of contextual information about a study episode that is encoded or retrieved, and not with the strength of an undifferentiated memory signal.

Overlap between the neural correlates of cued recall and source memory: evidence for a generic recollection network?

Recall of a studied item and retrieval of its encoding context (source memory) both depend on recollection of qualitative information about the study episode. This study investigated whether recall and source memory engage overlapping neural regions. Participants (n = 18) studied a series of words, which were presented either to the left or right of fixation. fMRI data were collected during a subsequent test phase in which three-letter word-stems were presented, two thirds of which could be completed by a study item. Instructions were to use each stem as a cue to recall a studied word and, when recall was successful, to indicate the word's study location. When recall failed, the stem was to be completed with the first word to come to mind. Relative to stems for which recall failed, word-stems eliciting successful recall were associated with enhanced activity in a variety of cortical regions, including bilateral parietal, posterior midline, and parahippocampal cortex. Activity in these regions was enhanced when recall was accompanied by successful rather than unsuccessful source retrieval. It is proposed that the regions form part of a "recollection network" in which activity is graded according to the amount of information retrieved about a study episode.

Comparison of the neural correlates of retrieval success in tests of cued recall and recognition memory.

The neural correlates of successful retrieval on tests of word stem recall and recognition memory were compared. In the recall test, subjects viewed word stems, half of which were associated with studied items and half with unstudied items, and for each stem attempted to recall a corresponding study word. In the recognition test, old/new judgments were made on old and new words. The neural correlates of successful retrieval were identified by contrasting activity elicited by correctly endorsed test items. Old > new effects common to the two tasks were found in medial and lateral parietal and right entorhinal cortex. Common new > old effects were identified in medial and left frontal cortex, and left anterior intra-parietal sulcus. Greater old > new effects were evident for cued recall in inferior parietal regions abutting those demonstrating common effects, whereas larger new > old effects were found for recall in left frontal cortex and the anterior cingulate. New > old effects were also found for the recall task in right lateral anterior prefrontal cortex, where they were accompanied by old > new effects during recognition. It is concluded that successful recall and recognition are associated with enhanced activity in a common set of recollection-sensitive parietal regions, and that the greater activation in these regions during recall reflects the greater dependence of that task on recollection. Larger new > old effects during recall are interpreted as reflections of the greater opportunity for iterative retrieval attempts when retrieval cues are partial rather than copy cues.

Left parietal cortex is modulated by amount of recollected verbal information.

In two earlier experiments, we reported that left parietal cortex activity covaried with the amount of pictorial information recollected. The present experiment addressed the question whether our earlier results would generalize to verbal materials. Participants studied a series of word pairs and were then tested on individual old and new words in a modified remember/know task. In this task, participants were required to indicate whether recollection was accompanied by retrieval of study pairmates or not. As before, we operationally defined 'amount recollected' as the contrast between these two types of remember response. We found that the same left parietal region previously identified as sensitive to amount of recollected pictorial information is also sensitive to amount of recollected verbal information.

An investigation of the effects of relative probability of old and new test items on the neural correlates of successful and unsuccessful source memory.

The present event-related fMRI study addressed the question whether retrieval-related neural activity in lateral parietal cortex is affected by the relative probability of test items. We varied the proportion of old to new items across two test blocks, with 25% of the items being old in one block and 75% being old in the other. Prior to each block, participants (N=18) completed one of two types of study judgment on each of 108 object images. They then performed a source memory test with four response options: studied in task 1, studied in task 2, old but unsure of the study task, and new. Retrieval-related activity in regions previously identified as recollection-sensitive, including the left inferior lateral parietal cortex and bilateral medial temporal cortex, was unaffected by old/new ratio. Generic retrieval success effects--retrieval-related effects common to recognized items attracting either a correct or an incorrect source judgment--were identified in several regions of left superior parietal cortex. These effects dissociated between a middle region of the intraparietal sulcus (IPS), where activity did not interact with ratio, and regions anterior and posterior to the middle IPS where activity was sensitive to old/new ratio. The findings are inconsistent with prior proposals that retrieval-related activity in and around the left middle IPS reflects the relative salience of old and new test items. Rather, they suggest that, as in the case of more inferior left parietal regions, retrieval-related activity in this region reflects processes directly linked to retrieval.

Functional significance of retrieval-related activity in lateral parietal cortex: Evidence from fMRI and ERPs.

The present study addressed the question whether neural activity in left lateral parietal cortex is modulated by amount of information recollected. In two experiments (one using fMRI and the other ERPs), subjects first studied pairs of pictures presented for either 1 or 6 s. They then performed a standard "Remember/Know" recognition memory test in which the old items comprised one of the pictures from each studied pair. In both experiments, a surprise posttest indicated that subjects recollected more details about the study presentation of the items presented for the longer duration. In the fMRI experiment, recollection- and familiarity-based recognition elicited activity in distinct cortical networks. Additionally, recollection-related activity in left inferior parietal cortex was of greater magnitude for test items presented for 6 s than for 1 s. In the ERP study the "left-parietal old/new effect"-a putative correlate of successful recollection-was likewise modulated by amount of information retrieved. Together, these findings provide further support for dual-process models of recognition memory and add weight to the proposal that retrieval-related activity in left inferior parietal cortex reflects processes supporting the online representation of retrieved episodic information.

Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective.

Although regions of the parietal cortex have been consistently implicated in episodic memory retrieval, the functional roles of these regions remain poorly understood. The present review presents a meta-analysis of findings from event-related fMRI studies reporting the loci of retrieval effects associated with familiarity- and recollection-related recognition judgments. The results of this analysis support previous suggestions that retrieval-related activity in lateral parietal cortex dissociates between superior regions, where activity likely reflects the task relevance of different classes of recognition test items, and more inferior regions where retrieval-related activity appears closely linked to successful recollection. It is proposed that inferior lateral parietal cortex forms part of a neural network supporting the 'episodic buffer' [Baddeley, A. D. (2000). The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 4, 417-423].

Dissociation of the neural correlates of recognition memory according to familiarity, recollection, and amount of recollected information.

The present experiment used fMRI to investigate whether neural correlates of recognition memory behave in a manner consistent with the proposal that recognition decisions are based on a unidimensional memory strength variable. A modified Remember/Know recognition test was used in which participants could indicate two levels of recollection. Participants were required to indicate whether a test item was new, familiar (known), elicited recollection of general contextual details from the study episode (R1 response), or elicited a specific recollection of the item with which it was paired at study (R2 response). Little evidence could be found to support the view that Remember/Know/New judgments reflect variations along a single strength dimension. Instead, the findings replicated prior research in indicating that the neural correlates of recollection and familiarity can be doubly dissociated. Two recollection-sensitive regions - left lateral inferior parietal and left fusiform cortex - were found to be sensitive to amount of information recollected, as operationalized in the contrast between R2 and R1 responses. It is proposed that these regions may support the representation of recollected information.

The relationship between electrophysiological correlates of recollection and amount of information retrieved.

The electrophysiological correlates of recollection were investigated with a modified Remember/Know task in which subjects signaled whether they fully or partially recollected visual object information in each study episode. A positive-going ERP deflection--the left parietal old/new effect--was sensitive to the amount of information recollected, demonstrating greater amplitude when elicited by test items associated with full relative to partial recollection. These findings support prior proposals that the left parietal ERP old/new effect is sensitive to the amount of information recollected from episodic memory. An early-onsetting (ca. 150 ms), left frontal old/new effect differentiated items accorded correct old versus correct new responses regardless of whether the items were endorsed as familiar or recollected. This finding extends the range of circumstances under which early, frontally distributed old/new effects occur, and adds weight to previous suggestions that these effects are a neural correlate of familiarity-driven recognition memory.

Identifying the ERP correlate of a recognition memory search attempt.

Previous recognition memory studies have looked for differences in brain activity during recollection- and familiarity-based responding. Although an ERP component correlated with recollection success has been reported, no analogous component related to search initiation has been found. We argue that such a component has not been discovered because studies have compared trials in which participants have made a search attempt and failed (such as Know responses) with those in which the search attempt is successful (such as Remember responses). In the current study, we compared a task that required judgments of lifetime familiarity (differentiating famous from nonfamous names) with one that required judgments of episodic information (deciding whether a name was seen previously in the experiment). By comparing a task on which familiarity judgments were made with no search attempt to a second task in which a search attempt was likely to occur, we identified a component that may reflect the initiation of a memory search. This effect, maximal between 190 and 235 ms, is correlated with Old judgments in the episodic task. Previous ERP findings (e.g., FN400, parietal old/new effect) were also replicated in the present study.