Reduced memory precision in older age is associated with functional and structural differences in the angular gyrus.

Decreased fidelity of mnemonic representations plays a critical role in age-related episodic memory deficits, yet the brain mechanisms underlying such reductions remain unclear. Using functional and structural neuroimaging, we examined how changes in two key nodes of the posterior-medial network, the hippocampus and the angular gyrus (AG), might underpin loss of memory precision in older age. Healthy young and older adults completed a memory task that involved reconstructing object features on a continuous scale. Investigation of blood-oxygen-level-dependent (BOLD) activity during retrieval revealed an age-related reduction in activity reflecting successful recovery of object features in the hippocampus, whereas trial-wise modulation of BOLD signal by graded memory precision was diminished in the AG. Gray matter volume of the AG further predicted individual differences in memory precision in older age, beyond likelihood of successful retrieval. These findings provide converging evidence for a role of functional and structural integrity of the AG in constraining the fidelity of episodic remembering in older age, yielding new insights into parietal contributions to age-related episodic memory decline.

Episodic Memory Precision and Reality Monitoring Following Stimulation of Angular Gyrus.

The qualities of remembered experiences are often used to inform "reality monitoring" judgments, our ability to distinguish real and imagined events. Previous experiments have tended to investigate only whether reality monitoring decisions are accurate or not, providing little insight into the extent to which reality monitoring may be affected by qualities of the underlying mnemonic representations. We used a continuous-response memory precision task to measure the quality of remembered experiences that underlie two different types of reality monitoring decisions: self/experimenter decisions that distinguish actions performed by participants and the experimenter and imagined/perceived decisions that distinguish imagined and perceived experiences. The data revealed memory precision to be associated with higher accuracy in both self/experimenter and imagined/perceived reality monitoring decisions, with lower precision linked with a tendency to misattribute self-generated experiences to external sources. We then sought to investigate the possible neurocognitive basis of these observed associations by applying brain stimulation to a region that has been implicated in precise recollection of personal events, the left angular gyrus. Stimulation of angular gyrus selectively reduced the association between memory precision and self-referential reality monitoring decisions, relative to control site stimulation. The angular gyrus may, therefore, be important for the mnemonic processes involved in representing remembered experiences that give rise to a sense of self-agency, a key component of "autonoetic consciousness" that characterizes episodic memory.

Hippocampal-Cortical Encoding Activity Predicts the Precision of Episodic Memory.

Our recollections of past experiences can vary in both the number of specific event details accessible from memory and the precision with which such details are reconstructed. Prior neuroimaging evidence suggests the success and precision of episodic recollection to rely on distinct neural substrates during memory retrieval. In contrast, the specific encoding mechanisms supporting later memory precision, and whether they differ from those underlying successful memory formation in general, are currently unknown. Here, we combined continuous measures of memory retrieval with model-based analyses of behavioral and neuroimaging data to tease apart the encoding correlates of successful memory formation and mnemonic precision. In the MRI scanner, participants encoded object-scene displays and later reconstructed features of studied objects using a continuous scale. We observed overlapping encoding activity in inferior prefrontal and posterior perceptual regions to predict both which object features were later remembered versus forgotten and the precision with which they were reconstructed from memory. In contrast, hippocampal encoding activity significantly predicted the precision, but not overall success, of subsequent memory retrieval. The current results align with theoretical accounts proposing the hippocampus to be critical for representation of high-fidelity associative information and suggest a contribution of shared cortical encoding mechanisms to the formation of both accessible and precise memory representations.

Healthy ageing reduces the precision of episodic memory retrieval.

Episodic memory declines with older age, but it is unresolved whether this decline reflects reduced probability of successfully retrieving information from memory, or decreased precision of the retrieved information. Here, we used continuous measures of episodic memory retrieval in combination with computational mixture modeling of participants' retrieval errors to distinguish between these two potential accounts of age-related memory deficits. In three experiments, young and older participants encoded stimulus displays consisting of everyday objects varying along different perceptual features (e.g., location, color and orientation) in a circular space. At test, participants recreated the features of studied objects using a continuous response dial. Across all 3 experiments, we observed significant age-related declines in the precision of episodic memory retrieval, whereas significant age differences in retrieval success were limited to the most challenging task condition. Reductions in mnemonic precision were evident across different object features retained in long-term memory and persisted after controlling for age-related decreases in the fidelity of perception and working memory. The findings highlight impoverished precision of memory representations as one factor contributing to age-related episodic memory loss and suggest that the cognitive and neural changes associated with older age may differentially affect distinct aspects of episodic retrieval. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Interference between overlapping memories is predicted by neural states during learning.

One of the primary contributors to forgetting is interference from overlapping memories. Intuitively, this suggests-and prominent theoretical models argue-that memory interference is best avoided by encoding overlapping memories as if they were unrelated. It is therefore surprising that reactivation of older memories during new encoding has been associated with reduced memory interference. Critically, however, prior studies have not directly established why reactivation reduces interference. Here, we first developed a behavioral paradigm that isolates the negative influence that overlapping memories exert during memory retrieval. We then show that reactivating older memories during the encoding of new memories dramatically reduces this interference cost at retrieval. Finally, leveraging multiple fMRI decoding approaches, we show that spontaneous reactivation of older memories during new encoding leads to integration of overlapping memories and, critically, that integration during encoding specifically reduces interference between overlapping, and otherwise competing, memories during retrieval.

Flexible updating of dynamic knowledge structures.

Schemas are knowledge structures that allow us to make efficient judgments about the world without the cost of memorizing every detail of previous experiences. It has long been known that schemas can enhance long-term memory for related information. The usefulness of schemas, however, critically depends on their adaptability: how flexibly a schema can be updated according to changing environmental conditions. Prior consolidation of a schema supports new learning of schema-consistent information. Yet, the effect of consolidation on inconsistent information, and how schemas may be subsequently updated, are not well understood. It is difficult to track the dynamic updating of knowledge structures with traditional memory measures. Here, using a continuous-report paradigm, we were able to show that schematization increases incrementally with consolidation and that the strength with which schemas are initially established predicts schema-guided responding in a later test. Critically, schema updating in response to inconsistent information was more pronounced in a group which was given time to consolidate compared to a group that was not given time to consolidate. Importantly, the later group reverted back to the no longer relevant schema, indicating that systematic bias towards old information, rather than increased forgetting, underlies reduced memory for schema-inconsistent information.

Decomposing Parietal Memory Reactivation to Predict Consequences of Remembering.

Memory retrieval can strengthen, but also distort memories. Parietal cortex is a candidate region involved in retrieval-induced memory changes as it reflects retrieval success and represents retrieved content. Here, we conducted an fMRI experiment to test whether different forms of parietal reactivation predict distinct consequences of retrieval. Subjects studied associations between words and pictures of faces, scenes, or objects, and then repeatedly retrieved half of the pictures, reporting the vividness of the retrieved pictures ("retrieval practice"). On the following day, subjects completed a recognition memory test for individual pictures. Critically, the test included lures highly similar to studied pictures. Behaviorally, retrieval practice increased both hit and false alarm (FA) rates to similar lures, confirming a causal influence of retrieval on subsequent memory. Using pattern similarity analyses, we measured two different levels of reactivation during retrieval practice: generic "category-level" reactivation and idiosyncratic "item-level" reactivation. Vivid remembering during retrieval practice was associated with stronger category- and item-level reactivation in parietal cortex. However, these measures differentially predicted subsequent recognition memory performance: whereas higher category-level reactivation tended to predict FAs to lures, item-level reactivation predicted correct rejections. These findings indicate that parietal reactivation can be decomposed to tease apart distinct consequences of memory retrieval.

Reduced Hippocampal Functional Connectivity During Episodic Memory Retrieval in Autism.

Increasing recent research has sought to understand the recollection impairments experienced by individuals with autism spectrum disorder (ASD). Here, we tested whether these memory deficits reflect a reduction in the probability of retrieval success or in the precision of memory representations. We also used functional magnetic resonance imaging (fMRI) to study the neural mechanisms underlying memory encoding and retrieval in ASD, focusing particularly on the functional connectivity of core episodic memory networks. Adults with ASD and typical control participants completed a memory task that involved studying visual displays and subsequently using a continuous dial to recreate their appearance. The ASD group exhibited reduced retrieval success, but there was no evidence of a difference in retrieval precision. fMRI data revealed similar patterns of brain activity and functional connectivity during memory encoding in the 2 groups, though encoding-related lateral frontal activity predicted subsequent retrieval success only in the control group. During memory retrieval, the ASD group exhibited attenuated lateral frontal activity and substantially reduced hippocampal connectivity, particularly between hippocampus and regions of the fronto-parietal control network. These findings demonstrate notable differences in brain function during episodic memory retrieval in ASD and highlight the importance of functional connectivity to understanding recollection-related retrieval deficits in this population.

ERP Correlates of Encoding Success and Encoding Selectivity in Attention Switching.

Long-term memory encoding depends critically on effective processing of incoming information. The degree to which participants engage in effective encoding can be indexed in electroencephalographic (EEG) data by studying event-related potential (ERP) subsequent memory effects. The current study investigated ERP correlates of memory success operationalised with two different measures-memory selectivity and global memory-to assess whether previously observed ERP subsequent memory effects reflect focused encoding of task-relevant information (memory selectivity), general encoding success (global memory), or both. Building on previous work, the present study combined an attention switching paradigm-in which participants were presented with compound object-word stimuli and switched between attending to the object or the word across trials-with a later recognition memory test for those stimuli, while recording their EEG. Our results provided clear evidence that subsequent memory effects resulted from selective attentional focusing and effective top-down control (memory selectivity) in contrast to more general encoding success effects (global memory). Further analyses addressed the question of whether successful encoding depended on similar control mechanisms to those involved in attention switching. Interestingly, differences in the ERP correlates of attention switching and successful encoding, particularly during the poststimulus period, indicated that variability in encoding success occurred independently of prestimulus demands for top-down cognitive control. These results suggest that while effects of selective attention and selective encoding co-occur behaviourally their ERP correlates are at least partly dissociable.

Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory.

A network of brain regions have been linked with episodic memory retrieval, but limited progress has been made in identifying the contributions of distinct parts of the network. Here, we utilized continuous measures of retrieval to dissociate three components of episodic memory: retrieval success, precision, and vividness. In the fMRI scanner, participants encoded objects that varied continuously on three features: color, orientation, and location. Participants' memory was tested by having them recreate the appearance of the object features using a continuous dial, and continuous vividness judgments were recorded. Retrieval success, precision, and vividness were dissociable both behaviorally and neurally: successful versus unsuccessful retrieval was associated with hippocampal activity, retrieval precision scaled with activity in the angular gyrus, and vividness judgments tracked activity in the precuneus. The ability to dissociate these components of episodic memory reveals the benefit afforded by measuring memory on a continuous scale, allowing functional parcellation of the retrieval network.

Multimodal Feature Integration in the Angular Gyrus during Episodic and Semantic Retrieval.

UNLABELLED: Much evidence from distinct lines of investigation indicates the involvement of angular gyrus (AnG) in the retrieval of both episodic and semantic information, but the region's precise function and whether that function differs across episodic and semantic retrieval have yet to be determined. We used univariate and multivariate fMRI analysis methods to examine the role of AnG in multimodal feature integration during episodic and semantic retrieval. Human participants completed episodic and semantic memory tasks involving unimodal (auditory or visual) and multimodal (audio-visual) stimuli. Univariate analyses revealed the recruitment of functionally distinct AnG subregions during the retrieval of episodic and semantic information. Consistent with a role in multimodal feature integration during episodic retrieval, significantly greater AnG activity was observed during retrieval of integrated multimodal episodic memories compared with unimodal episodic memories. Multivariate classification analyses revealed that individual multimodal episodic memories could be differentiated in AnG, with classification accuracy tracking the vividness of participants' reported recollections, whereas distinct unimodal memories were represented in sensory association areas only. In contrast to episodic retrieval, AnG was engaged to a statistically equivalent degree during retrieval of unimodal and multimodal semantic memories, suggesting a distinct role for AnG during semantic retrieval. Modality-specific sensory association areas exhibited corresponding activity during both episodic and semantic retrieval, which mirrored the functional specialization of these regions during perception. The results offer new insights into the integrative processes subserved by AnG and its contribution to our subjective experience of remembering. SIGNIFICANCE STATEMENT: Using univariate and multivariate fMRI analyses, we provide evidence that functionally distinct subregions of angular gyrus (AnG) contribute to the retrieval of episodic and semantic memories. Our multivariate pattern classifier could distinguish episodic memory representations in AnG according to whether they were multimodal (audio-visual) or unimodal (auditory or visual) in nature, whereas statistically equivalent AnG activity was observed during retrieval of unimodal and multimodal semantic memories. Classification accuracy during episodic retrieval scaled with the trial-by-trial vividness with which participants experienced their recollections. Therefore, the findings offer new insights into the integrative processes subserved by AnG and how its function may contribute to our subjective experience of remembering.

Predicting the integration of overlapping memories by decoding mnemonic processing states during learning.

The hippocampal memory system is thought to alternate between two opposing processing states: encoding and retrieval. When present experience overlaps with past experience, this creates a potential tradeoff between encoding the present and retrieving the past. This tradeoff may be resolved by memory integration-that is, by forming a mnemonic representation that links present experience with overlapping past experience. Here, we used fMRI decoding analyses to predict when - and establish how - past and present experiences become integrated in memory. In an initial experiment, we alternately instructed subjects to adopt encoding, retrieval or integration states during overlapping learning. We then trained across-subject pattern classifiers to 'read out' the instructed processing states from fMRI activity patterns. We show that an integration state was clearly dissociable from encoding or retrieval states. Moreover, trial-by-trial fluctuations in decoded evidence for an integration state during learning reliably predicted behavioral expressions of successful memory integration. Strikingly, the decoding algorithm also successfully predicted specific instances of spontaneous memory integration in an entirely independent sample of subjects for whom processing state instructions were not administered. Finally, we show that medial prefrontal cortex and hippocampus differentially contribute to encoding, retrieval, and integration states: whereas hippocampus signals the tradeoff between encoding vs. retrieval states, medial prefrontal cortex actively represents past experience in relation to new learning.

Corresponding influences of top-down control on task switching and long-term memory.

Three experiments investigated the impact of cognitive control on current performance and later memory in task switching. Participants first switched between object and word classification tasks, performed on picture-word stimuli that each appeared only once, then were tested for their recognition memory of these items. Each experiment replicated the recent finding that task switching results in reduced selectivity in later memory for task-relevant over task-irrelevant items. Top-down control was manipulated through varying the time available for advance task preparation (Experiment 1), the freedom of choice over which task to perform (Experiment 2), and the availability of reward incentives (Experiment 3). For each manipulation, more effective top-down control during task switching was associated with increased selectivity in memory for task-relevant information. These findings shed new light on the role of cognitive control in long-term memory encoding, in particular supporting an interactive model in which long-term memory reflects the enduring traces of perceptual and cognitive processes that operate under the selective influence of top-down control.

Memory and cognitive control in task switching.

Cognitive control and memory are fundamentally intertwined, but interactions between the two have only recently received sustained research interest. In the study reported here, we used a novel paradigm to investigate how control influences memory encoding and, conversely, how memory measures can provide new insight into flexible cognitive control. Participants switched between classifying objects and words, then were tested for their recognition memory of items presented in this task-switching phase. Task switching impaired memory for task-relevant information but actually improved memory for task-irrelevant information, which indicates that control demands reduced the selectivity of memory encoding rather than causing a general memory decline. Recognition memory strength provided a robust trial-by-trial measure of the effectiveness of cognitive control that "predicted" earlier task-switching performance. It also revealed a substantial influence of bottom-up factors on between-task competition, but only on trials in which participants had to switch from one type of classification to the other. Collectively, our findings illustrate how cognitive control and bottom-up factors interact to simultaneously influence both current performance and future memory.

Controlling conflict from interfering long-term memory representations.

Remembering is more than an activation of a memory trace. As retrieval cues are often not uniquely related to one specific memory, cognitive control should come into play to guide selective memory retrieval by focusing on relevant while ignoring irrelevant information. Here, we investigated, by means of EEG and fMRI, how the memory system deals with retrieval interference arising when retrieval cues are associated with two material types (faces and spatial positions), but only one is task-relevant. The topography of slow EEG potentials and the fMRI BOLD signal in posterior storage areas indicated that in such situations not only the relevant but also the irrelevant material becomes activated. This results in retrieval interference that triggers control processes mediated by the medial and lateral PFC, which are presumably involved in biasing target representations by boosting the task-relevant material. Moreover, memory-based conflict was found to be dissociable from response conflict that arises when the relevant and irrelevant materials imply different responses. The two types of conflict show different activations in the medial frontal cortex, supporting the claim of domain-specific prefrontal control systems.