Neural Correlates Of Recollection Research Articles

The late positive event-related potential component is time locked to the decision in recognition memory tasks

Two event-related potential (ERP) components are commonly observed in recognition memory tasks: the Frontal Negativity (FN400) and the Late Positive Component (LPC). These components are widely interpreted as neural correlates of familiarity and recollection, respectively. However, the interpretation of LPC effects is complicated by inconsistent results regarding the timing of ERP amplitude differences. There are also mixed findings regarding how LPC amplitudes covary with decision confidence. Critically, LPC effects have almost always been measured using fixed time windows relative to memory probe stimulus onset, yet it has not been determined whether LPC effects are time locked to the stimulus or the recognition memory decision. To investigate this, we analysed a large (n = 132) existing dataset recorded during recognition memory tasks with old/new decisions followed by post-decisional confidence ratings. We used ERP deconvolution to disentangle contributions to LPC effects (defined as differences between hits and correct rejections) that were time locked to either the stimulus or the vocal old/new response. We identified a left-lateralised parietal LPC effect that was time locked to the vocal response rather than probe stimulus onset. We also isolated a response-locked, midline parietal ERP correlate of confidence that influenced measures of LPC amplitudes at left parietal electrodes. Our findings demonstrate that, contrary to widespread assumptions, the LPC effect is time locked to the recognition memory decision and is best measured using response-locked ERPs. By extension, differences in response time distributions across conditions of interest may lead to substantial measurement biases when analysing stimulus-locked ERPs. Our findings highlight important confounding factors that further complicate the interpretation of existing stimulus-locked LPC effects as neural correlates of recollection. We recommend that future studies adopt our analytic approach to better isolate LPC effects and their sensitivity to manipulations in recognition memory tasks.

Age differences in the neural correlates of recollection: transient versus sustained fMRI effects

Prior functional magnetic resonance imaging findings in young adults indicate that recollection-sensitive neural regions dissociate according to the time courses of their respective recollection effects. Here, we examined whether such dissociations are also evident in older adults. Young and older participants encoded a series of word-image pairs, judging which of the denoted objects was the smaller. At the test, participants judged whether each of a series of test words was old or new. If a word was old, the requirement was to recall the associated image and maintain it over a variable delay period. Older adults demonstrated significantly lower associative memory performance than young adults. Transient recollection effects were identified in the left hippocampus, medial prefrontal cortex, and posterior cingulate, while sustained effects were widespread across left lateral cortex and were also evident in the bilateral striatum. Except for those in the left insula, all effects were age-invariant. These findings suggest that both transient and sustained recollection effects are largely stable across much of the healthy adult life span.

Age differences in the neural correlates of the specificity of recollection: An event-related potential study

In young adults, the neural correlates of successful recollection vary with the specificity (or amount) of information retrieved. We examined whether the neural correlates of recollection are modulated in a similar fashion in older adults. We compared event-related potential (ERP) correlates of recollection in samples of healthy young and older adults (N = 20 per age group). At study, participants were cued to make one of two judgments about each of a series of words. Subsequently, participants completed a memory test for studied and unstudied words in which they first made a Remember/Know/New (RKN) judgment, followed by a source memory judgment when a word attracted a ‘Remember’ (R) response. In young adults, the ‘left parietal effect’ – a putative ERP correlate of successful recollection – was largest for test items endorsed as recollected (R judgment) and attracting a correct source judgment, intermediate for items endorsed as recollected but attracting an incorrect or uncertain source judgment, and, relative to correct rejections, absent for items endorsed as familiar only (K judgment). In marked contrast, the left parietal effect was not detectable in older adults. Rather, regardless of source accuracy, studied items attracting an R response elicited a sustained, centrally maximum negative-going deflection relative to both correct rejections and studied items where recollection failed (K judgment). A similar retrieval-related negativity has been described previously in older adults, but the present findings are among the few to link this effect specifically to recollection. Finally, relative to correct rejections, all classes of correctly recognized old items elicited an age-invariant, late-onsetting positive deflection that was maximal over the right frontal scalp. This finding, which replicates several prior results, suggests that post-retrieval monitoring operations were engaged to an equivalent extent in the two age groups. Together, the present results suggest that there are circumstances where young and older adults engage qualitatively distinct retrieval-related processes during successful recollection.

Network-targeted stimulation engages neurobehavioral hallmarks of age-related memory decline.

To test whether targeting hippocampal-cortical brain networks with high-frequency transcranial magnetic stimulation in older adults influences behavioral and neural measures characteristic of age-related memory impairment. Fifteen adults aged 64 to 80 years (mean = 72 years) completed a single-blind, sham-controlled experiment. Stimulation targets in parietal cortex were determined based on fMRI connectivity with the hippocampus. Recollection and recognition memory were assessed after 5 consecutive daily sessions of full-intensity stimulation vs low-intensity sham stimulation using a within-subjects crossover design. Neural correlates of recollection and recognition memory formation were obtained via fMRI, measured within the targeted hippocampal-cortical network vs a control frontal-parietal network. These outcomes were measured approximately 24 hours after the final stimulation session. Recollection was specifically impaired in older adults compared to a young-adult control sample at baseline. Relative to sham, stimulation improved recollection to a greater extent than recognition. Stimulation increased recollection fMRI signals throughout the hippocampal-cortical network, including at the targeted location of the hippocampus. Effects of stimulation on fMRI recollection signals were greater than those for recognition and were greater in the targeted network compared to the control network. Age-related recollection impairments were causally related to hippocampal-cortical network function in older adults. Stimulation selectively modified neural and behavioral hallmarks of age-related memory impairment, indicating effective engagement of memory intervention targets in older adults.

Dissociation between the neural correlates of recollection and familiarity in the striatum and hippocampus: Across-study convergence

In tests of recognition memory, neural activity in the striatum has consistently been reported to differ according to the study status of the test item. A full understanding of the functional significance of striatal ‘retrieval success’ effects is impeded by a paucity of evidence concerning whether the effects differ according to the nature of the memory signal supporting the recognition judgment (recollection vs. familiarity). Here, we address this issue through an analysis of retrieval-related striatal activity in three independent fMRI studies (total N = 88). Recollection and familiarity were operationalized in a different way in each study, allowing the identification of test-independent, generic recollection- and familiarity-related effects. While activity in a bilateral dorsal striatal region, mainly encompassing the caudate nucleus, was enhanced equally by recollected and ‘familiar only’ test items, activity in bilateral ventral striatum and adjacent subgenual frontal cortex was enhanced only in response to items that elicited successful recollection. By contrast, relative to familiar items, activity in anterior hippocampus was enhanced for both recollected and novel test items. Thus, recollection- and familiarity-driven recognition memory judgments are associated with anatomically distinct patterns of retrieval-related striatal activity, and these patterns are at least partially independent of recollection and novelty effects in the hippocampus.

Retrieval Orientation and the Control of Recollection: An fMRI Study

This study used event-related fMRI to examine the impact of the adoption of different retrieval orientations on the neural correlates of recollection. In each of two study-test blocks, participants encoded a mixed list of words and pictures and then performed a recognition memory task with words as the test items. In one block, the requirement was to respond positively to test items corresponding to studied words and to reject both new items and items corresponding to the studied pictures. In the other block, positive responses were made to test items corresponding to pictures, and items corresponding to words were classified along with the new items. On the basis of previous ERP findings, we predicted that in the word task, recollection-related effects would be found for target information only. This prediction was fulfilled. In both tasks, targets elicited the characteristic pattern of recollection-related activity. By contrast, nontargets elicited this pattern in the picture task, but not in the word task. Importantly, the left angular gyrus was among the regions demonstrating this dissociation of nontarget recollection effects according to retrieval orientation. The findings for the angular gyrus parallel prior findings for the "left-parietal" ERP old/new effect and add to the evidence that the effect reflects recollection-related neural activity originating in left ventral parietal cortex. Thus, the results converge with the previous ERP findings to suggest that the processing of retrieval cues can be constrained to prevent the retrieval of goal-irrelevant information.

A Rapid, Hippocampus-Dependent, Item-Memory Signal that Initiates Context Memory in Humans

SummaryThe hippocampus, a structure located in the temporal lobes of the brain, is critical for the ability to recollect contextual details of past episodes. It is still debated whether the hippocampus also enables recognition memory for previously encountered context-free items. Brain imaging [1, 2] and neuropsychological patient studies [3, 4] have both individually provided conflicting answers to this question. We overcame the individual limitations of imaging and behavioral patient studies by combining them and observed a novel relationship between item memory and the hippocampus. We show that interindividual variability of hippocampal volumes in a large patient population with graded levels of hippocampal volume loss and controls correlates with context, but not item-memory performance. Nevertheless, concurrent measures of brain activity using magnetoencephalography reveal an early (350 ms) but sustained hippocampus-dependent signal that evolves from an item signal into a context memory signal. This is temporally distinct from an item-memory signal that is not hippocampus dependent. Thus, we provide evidence for a hippocampus-dependent item-memory process that initiates context retrieval without making a substantial contribution to item recognition performance. Our results reconcile contradictory evidence concerning hippocampal involvement in item memory and show that hippocampus-dependent mnemonic processes are more rapid than previously believed.

Differential effects of aging on the neural correlates of recollection and familiarity

The present experiment aimed to investigate age differences in the neural correlates of familiarity and recollection, while keeping performance similar across age groups by varying task difficulty. Twenty young and 20 older adults performed an episodic memory task in an event-related functional magnetic resonance imaging (fMRI) design. At encoding, participants were presented with pictures, either once or twice. Then, they performed a recognition task, with a Remember/Know paradigm. A similar performance was observed for the two groups in the Easy condition for recollection and in the Hard condition for familiarity. Imaging data revealed the classic recollection-related and familiarity-related networks, common to young and older groups. In addition, we observed that some activity related to recollection (left frontal, left temporal, left parietal cortices and left parahippocampus) and familiarity (bilateral anterior cingulate, right frontal gyrus and left superior temporal gyrus) was reduced in older compared to young adults. However, for recollection processes only, older adults additionally recruited the right precuneus, possibly to successfully compensate for their difficulties, as suggested by a positive correlation between recollection and precuneus activity.

The neural correlates of recollection and familiarity during aging

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Reactivation of context-specific brain regions during retrieval

The neural correlates of recollection were examined using event-related functional MRI. We examined how the presence of different visual context information during encoding of target words influenced later recollection for the words presented alone at retrieval. Participants studied words presented with different pictures of faces or scrambled faces on each trial, and on a subsequent scanned recognition test made 'remember', 'know' or 'new' responses to words presented alone. Prior to the study phase, participants performed a localizer task, in which the fusiform face area (FFA) was identified. We compared brain activation patterns for remember and know responses given to words studied with faces as compared to scrambled faces. Though behaviourally participants showed no difference in memory performance depending on encoding trial type, both a group- and individual-based region-of-interest analysis showed increased activation in the functionally-defined FFA for remember responses given to words studied with faces compared to scrambled faces. A regression analysis additionally showed that activation in the right fusiform gyrus increased as the relative recollection benefit for words studied with meaningful (face) compared to non-meaningful (scrambled face) context information increased. Results suggest that context-specific brain regions implicated during encoding are recruited during retrieval, and that the degree to which participants activate context-specific brain regions during retrieval is related to a behavioural benefit in later recollection for target information presented alone.

The neural correlates of recollection: Hippocampal activation declines as episodic memory fades

Memories for certain events tend to linger in rich, vivid detail, and retrieval of these memories includes a sense of re-experiencing the details of the event. Most events, however, are not retained in any detailed way for more than a few days. According to one theory, the hippocampus plays a specific role in supporting episodic retrieval, that is, the re-experiencing of an event as part of one's personal past. This theory predicts that as episodic memories fade over time and are reduced to feelings of familiarity, activity in the hippocampus should no longer be associated with retrieval. We used high-resolution functional imaging to explore neural activity in medial temporal lobe subregions while participants performed a recognition task at both a short (10-min) and long (1-week) study-test delay. For each recognized item, subjects made "Remember/Know" judgments, allowing us to distinguish between items that were consistently episodic across the two tests and items that were initially episodic, but later became merely familiar. Our results demonstrate that activity in the subiculum is specifically associated with episodic recollection. Overall, recollected items were associated with higher activity in the subiculum than other items. For transiently recollected items, there was a decrease in subicular activity across the 1-week delay as memory faded from recollection to familiarity, whereas consistently recollected items were associated with enhanced subicular activity at both delays. These results provide evidence of a link between subicular activation and recollective experience.

Recollection and the Reinstatement of Encoding-Related Cortical Activity

The neural correlates of episodic memory retrieval ("recollection") differ according to the type of information contained in the recollected episode. Such content-specific recollection effects have been hypothesized to reflect the reinstatement of processes or representations active during encoding. Using event-related functional magnetic resonance imaging, we evaluated this hypothesis by directly contrasting the neural activity elicited during the encoding and subsequent recollection of words studied with one of 2 encoding tasks. Study words appearing on pictures of scenes required imagining the word's referent at any location within the scene, whereas words appearing on a blank background required generating a sentence that incorporated the word. On a later memory test, the neural correlates of recollection were operationalized by contrasting the activity elicited during correct "remember" versus "know" responses. Recollected words from the "scene" task elicited activity in regions of left occipital cortex and anterior fusiform gyrus that overlapped regions where encoding-related activity was greater for the scene than sentence task. Conversely, activity elicited by words recollected from the "sentence" task overlapped with a region of ventromedial frontal cortex where encoding-related activity was greater for the sentence task. These content-specific associations between encoding- and recollection-related neural activity strongly support the reinstatement hypothesis of episodic retrieval.

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.