Constructive Memory and Conscious Experience.

Episodic memory relies on constructive processes that support simulating novel future events by flexibly recombining elements of past experiences, and that can also give rise to memory errors. In recent studies, we have developed methods to characterize the cognitive and neural processes that support conscious experiences linked to this process of episodic recombination, both when people simulate novel future events and commit recombination-related memory errors. In this Perspective, we summarize recent studies that illustrate these phenomena, and discuss broader implications for characterizing the basis of conscious experiences associated with constructive memory from a cognitive neuroscience perspective.

The dead salmon strikes again: Reports of unconscious processing in the hippocampus may reflect Type-I error.

Steinkrauss and Slotnick (2024) reviewed neuroimaging studies linking the hippocampus with implicit memory. They conclude that there is no convincing evidence that the hippocampus is associated with implicit memory because prior studies are confounded by explicit memory (among other factors). Here, we ask a different yet equally important question: do reports of unconscious hippocampal activity reflect a Type-I error (i.e. a false positive)? We find that 39% of studies linking the hippocampus with implicit memory (7 of 18) do not report correcting for multiple comparisons. These results indicate that many unconscious hippocampal effects may reflect a Type-I error.

Prefrontal cortex-mediated inhibition supports face recognition.

Inhibitory processes are thought to be important for memory function. A recent behavioral study that employed a face recognition paradigm reported that participants made fewer "old" responses to highly similar faces than less similar faces, providing evidence that memory for faces may rely on related-item inhibition. However, these results could also be explained by a non-inhibitory recall-to-reject process. The current study sought to use fMRI connectivity analysis to distinguish between these hypotheses. Although both hypotheses predict correct rejection of highly similar faces will produce activity in the prefrontal cortex, the inhibition hypothesis predicts negative connectivity between the prefrontal cortex and regions associated with memory retrieval and face processing, whereas the recall-to-reject hypothesis predicts positive connectivity between these regions. During the study phase, participants were presented with male and female faces. During the test phase, they viewed old faces, related face morphs (20-80% similar to old faces), and new faces, and made "old"-"new" judgements. Correct rejection of highly similar face morphs was associated with increased activity in the right lateral prefrontal cortex and negative connectivity between this region and regions associated with face processing and memory retrieval. These results indicate that prefrontal cortex-mediated memory inhibition supports face recognition.

Impaired cognitive performance in older adults is associated with deficits in item memory and memory for object features.

Amnestic mild cognitive impairment (aMCI) is associated with damage to the perirhinal/entorhinal cortex, and consequently, deficits in item/object memory. However, cognitive assessments commonly used to identify individuals with aMCI require a clinician to administer and interpret the test. We developed a novel self-administered global cognitive assessment, called the Cognitive Assessment via Keyboard (CAKe). To assess the relationship between CAKe performance and perirhinal/entorhinal cortex-dependent memory function, participants completed the CAKe, a feature source memory task, and a context memory task. During the memory tasks, participants studied line drawings with either a green or orange internal color (feature memory runs) or external color (context memory runs) and then classified each item as old and previously presented with a "green" or "orange" color, or "new". CAKe scores were correlated with item memory accuracies and source memory accuracies on both tasks. Participants with 'impaired' CAKe performance had worse item memory and worse feature source memory accuracies than those with 'normal' CAKe performance. These results demonstrate specific deficits in item memory and feature source memory and suggest that our assessments may be a valid predictor of aMCI memory deficits.

Constructive episodic retrieval processes underlying memory distortion contribute to creative thinking and everyday problem solving.

Constructive episodic retrieval processes play an adaptive role in supporting divergent thinking (i.e., creatively combining diverse bits of information) and means-end problem solving (i.e., generating steps to solve a social problem). However, the constructive nature of episodic memory that supports these adaptive functions also leads to memory error. In three experiments we aimed to identify a direct link between divergent thinking and means-end problem solving - as assessed in the Alternative Uses Task (AUT) and Means-End Problem Solving (MEPS) task - with the generation of false memories in the Deese-Roediger-McDermott paradigm. In Experiment 1, we replicated prior findings where false memory was positively correlated with performance on the AUT, and also showed for the first time that increased performance in the MEPS task is associated with increased false recall. In Experiment 2, we demonstrated that the link between false recall and performance on the MEPS task did not extend to other forms of problem solving, as assessed with the Everyday Descriptions Task (EDT). In Experiment 3, we showed that when the EDT was preceded by the MEPS task in an attempt to influence participants to engage in a similar episodic-problem solving strategy, performance in both tasks was correlated with false memory. These findings provide evidence for a direct link between the adaptive benefits of constructive episodic processes, in the form of enhanced divergent creative thinking and problem solving, and costs, in the form of increased memory error.

Transcranial magnetic stimulation to the angular gyrus modulates the temporal dynamics of the hippocampus and entorhinal cortex.

Transcranial magnetic stimulation (TMS) delivered to the angular gyrus (AG) affects hippocampal function and associated behaviors (Thakral PP, Madore KP, Kalinowski SE, Schacter DL. Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking. 2020a. Proc Natl Acad Sci U S A. 117:12729-12740). Here, we examine if functional magnetic resonance imaging (fMRI)-guided TMS disrupts the gradient organization of temporal signal properties, known as the temporal organization, in the hippocampus (HPC) and entorhinal cortex (ERC). For each of 2 TMS sessions, TMS was applied to either a control site (vertex) or to a left AG target region (N = 18; 14 females). Behavioral measures were then administered, and resting-state scans were acquired. Temporal dynamics were measured by tracking change in the fMRI signal (i) "within" single voxels over time, termed single-voxel autocorrelation and (ii) "between" different voxels over time, termed intervoxel similarity. TMS reduced AG connectivity with the hippocampal target and induced more rapid shifting of activity in single voxels between successive time points, lowering the single-voxel autocorrelation, within the left anteromedial HPC and posteromedial ERC. Intervoxel similarity was only marginally affected by TMS. Our findings suggest that hippocampal-targeted TMS disrupts the functional properties of the target site along the anterior/posterior axis. Further studies should examine the consequences of altering the temporal dynamics of these medial temporal areas to the successful processing of episodic information under task demand.

Representing the Good and Bad: fMRI signatures during the encoding of multisensory positive, negative, and neutral events.

Few studies have examined how multisensory emotional experiences are processed and encoded into memory. Here, we aimed to determine whether, at encoding, activity within functionally-defined visual- and auditory-processing brain regions discriminated the emotional category (i.e., positive, negative, or neutral) of the multisensory (audio-visual) events. Participants incidentally encoded positive, negative, and neutral multisensory stimuli during event-related functional magnetic resonance imaging (fMRI). Following a 3-h post-encoding delay, their memory for studied stimuli was tested, allowing us to identify emotion-category-specific subsequent-memory effects focusing on medial temporal lobe regions (i.e., amygdala, hippocampus) and visual- and auditory-processing regions. We used a combination of univariate and multivoxel pattern fMRI analyses (MVPA) to examine emotion-category-specificity in mean activity levels and neural patterning, respectively. Univariate analyses revealed many more visual regions that showed negative-category-specificity relative to positive-category-specificity, and auditory regions only showed negative-category-specificity. These results suggest that negative emotion is more closely tied to information contained within sensory regions, a conclusion that was supported by the MVPA analyses. Functional connectivity analyses further revealed that the visual amplification of category-selective processing is driven, in part, by mean signal from the amygdala. Interestingly, while stronger representations in visuo-auditory regions were related to subsequent-memory for neutral multisensory stimuli, they were related to subsequent-forgetting of positive and negative stimuli. Neural patterning in the hippocampus and amygdala were related to memory for negative multisensory stimuli. These results provide new evidence that negative emotional stimuli are processed with increased engagement of visuosensory regions, but that this sensory engagement-that generalizes across the entire emotion category-is not the type of sensory encoding that is most beneficial for later retrieval.

Sensitivity of the hippocampus to objective but not subjective episodic memory judgments.

We assessed whether neural activity in the hippocampus dissociates according to whether memory test items elicit a subjective sense of recollection or accurate retrieval of contextual information. We reanalyzed a previously acquired dataset from a study in which participants made both objective (source memory for spatial context) and subjective (Remember-Know) judgments for each test item. Results indicated that the hippocampus was exclusively sensitive to the amount of contextual information retrieved, such that accurate source memory judgments were associated with greater activity than inaccurate judgments, regardless of Remember/Know status. The findings add to the evidence that the hippocampus is insensitive to the subjective experience of recollection, but supports retrieval of contextual information.

Decoding the emotional valence of future thoughts.

Affective future thinking allows us to prepare for future outcomes, but we know little about neural representation of emotional future simulations. We used a multi-voxel pattern analysis to determine whether patterns of neural activity can reliably distinguish between positive and negative future simulations. Neural patterning in the anterior cingulate and ventromedial prefrontal cortices distinguished positive from negative future simulations, indicating that these regions code for the emotional valence of future events. These results support prior findings that anterior medial regions contain representations of emotions across various stimuli, and contribute to identifying potential rewarding outcomes of future events. More broadly, these results demonstrate that the phenomenological features of future thinking can be decoded using neural activity.

Linking creativity and false memory: Common consequences of a flexible memory system.

Episodic retrieval plays a functional-adaptive role in supporting divergent thinking, the ability to creatively combine different pieces of information. However, the same constructive memory process that provides a functional-adaptive benefit can also leave memory prone to error. In two experiments, we employed an individual differences approach to examine the relationship between different forms of creative thinking (divergent and convergent thinking) and false memory generation in the Deese-Roediger-McDermott paradigm. In Experiment 1, and replicating prior findings, false recognition was significantly predicted by convergent thinking performance. Critically, we also observed a novel predictive relationship between false recognition and quantitative metrics of divergent thinking performance. In Experiment 2, these findings were replicated and we further showed that false recall was predicted by quantitative metrics of divergent thinking. Our findings suggest that constructive memory processes link creative thinking with the production of memory errors.

Distinct patterns of hippocampal activity associated with color and spatial source memory.

The hippocampus is known to be involved in source memory across a wide variety of stimuli and source types. Thus, source memory activity in the hippocampus is thought to be domain-general such that different types of source information are similarly processed in the hippocampus. However, there is some evidence of domain-specificity for spatial and temporal source information. The current fMRI study aimed to determine whether patterns of activity in the hippocampus differed for two types of visual source information: spatial location and background color. Participants completed three runs of a spatial memory task and three runs of a color memory task. During the study phase, 32 line drawings of common objects and animals were presented to either the left or right of fixation for the spatial memory task or on either a red or green background for the color memory task. During the test phase of both tasks, 48 object word labels were presented in the center of the screen and participants classified the corresponding item as old and previously on the "left"/on a "green" background, old and previously on the "right"/on a "red" background, or "new." Two analysis methods were employed to assess whether hippocampal activity differed between the two source types: a general linear model analysis and a classification-based searchlight multivoxel pattern analysis (MVPA). The searchlight MVPA revealed that activity associated with spatial memory and color memory could be classified with above-chance accuracy in a region of the right anterior hippocampus, and a follow-up analysis revealed that there was a significant effect of memory accuracy. These results indicate that different types of source memory are represented by distinct patterns of activity in the hippocampus.

Divergent thinking and constructing future events: dissociating old from new ideas.

Divergent thinking (the ability to generate creative ideas by combining diverse types of information) has been previously linked to the ability to imagine novel and specific future autobiographical events. Here, we examined whether divergent thinking is differentially associated with the ability to construct novel imagined future events and recast future events (i.e., actual past events recast as future events) as opposed to recalled past events. We also examined whether different types of creative ideas (i.e., old ideas from memory or new ideas from imagination) underlie the linkage between divergent thinking and various autobiographical events. Divergent thinking ability was measured using the Alternate Uses Task (AUT). In Experiment 1, the amount of episodic details for both novel and recast future events was associated with divergent thinking (AUT scores), and this relationship was significant with AUT scores for new creative ideas but not old creative ideas. There was no significant relationship between divergent thinking and the amount of episodic detail for recalled past events. We extended these findings in Experiment 2 to a different test of divergent thinking, the Consequences Task. These results demonstrate that individual differences in divergent thinking are associated with the capacity to both imagine and recast future events.

Reinstatement of item-specific contextual details during retrieval supports recombination-related false memories.

Flexible retrieval mechanisms that allow us to infer relationships across events may also lead to memory errors or distortion when details of one event are misattributed to the related event. Here, we tested how making successful inferences alters representation of overlapping events, leading to false memories. Participants encoded overlapping associations ('AB' and 'BC'), each of which was superimposed on different indoor and outdoor scenes that were pre-exposed prior to associative learning. Participants were subsequently tested on both the directly learned pairs ('AB' and 'BC') and inferred relationships across pairs ('AC'). We predicted that when people make a correct inference, features associated with overlapping events may become integrated in memory. To test this hypothesis, participants completed a final detailed retrieval test, in which they had to recall the scene associated with initially learned 'AB' pairs (or 'BC' pairs). We found that the outcome of inference decisions impacted the degree to which neural patterns elicited during detailed 'AB' retrieval reflected reinstatement of the scene associated with the overlapping 'BC' event. After successful inference, neural patterns in the anterior hippocampus, posterior medial prefrontal cortex, and our content-reinstatement region (left inferior temporal gyrus) were more similar to the overlapping, yet incorrect 'BC' context relative to after unsuccessful inference. Further, greater hippocampal activity during inference was associated with greater reinstatement of the incorrect, overlapping context in our content-reinstatement region, which in turn tracked contextual misattributions during detailed retrieval. These results suggest recombining memories during successful inference can lead to misattribution of contextual details across related events, resulting in false memories.

High confidence spatial long-term memories produce greater cortical activity in males than females.

Many functional resonance imaging (fMRI) studies have reported sex differences during long-term memory. The present fMRI investigation aimed to identify whether sex differences exist during high- versus low-confidence accurate spatial memories. During the study phase, abstract shapes were presented to the left or right of fixation. During the test phase, each shape was presented at fixation and participants made an old-"left" or old-"right" judgment followed by an "unsure" or "sure" response. The conjunction of female high- versus low-confidence spatial memory and male high- versus low-confidence spatial memory identified common activity in visual processing regions and parietal cortex, which suggests amplification of activity in some of the regions commonly associated with long-term memory yields high confidence. The contrast of female high- versus low-confidence spatial memory and male high- versus low-confidence spatial memory did not produce any significant activity. However, the reverse contrast produced greater male than female activity in the lateral prefrontal cortex, parietal cortex, sensorimotor cortex, and visual processing regions. An independent region-of-interest (ROI) analysis (ROIs were identified by contrasting hits versus misses) produced complementary results in the lateral prefrontal cortex. Greater lateral prefrontal cortex activity suggests a higher degree of subjective confidence in males than females, greater parietal cortex and visual processing activity suggests more vivid visualization in males than females, and greater activity in sensorimotor cortex indicates that males have a more reactive processing style than females. More broadly, the present and previous functional sex differences argue against the practice of collapsing across sex in cognitive neuroscience studies.

Age-related changes in repetition suppression of neural activity during emotional future simulation.

Despite advances in understanding the consequences of age-related episodic memory decline for future simulation, much remains unknown regarding changes in the neural underpinnings of future thinking with age. We used a repetition suppression paradigm to explore age-related changes in the neural correlates of emotional future simulation. Younger and older adults simulated positive, negative, and neutral future events either 2 or 5 times. Reductions in neural activity for events simulated 5 versus 2 times (i.e., repetition suppression) identify brain regions responsive to the specific emotion of simulated events. Critically, older adults showed greater repetition suppression than younger adults in the temporal pole for negative simulations, and the cuneus for positive simulations. These findings suggest that older adults distance themselves from negative future possibilities by thinking about them in a more semantic way, consistent with the view that older adults down-regulate negative affect and up-regulate positive affect. More broadly this study increases our understanding of the impact of aging on the neural underpinnings of episodic future simulation.

Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking.

Prior functional magnetic resonance imaging (fMRI) studies indicate that a core network of brain regions, including the hippocampus, is jointly recruited during episodic memory, episodic simulation, and divergent creative thinking. Because fMRI data are correlational, it is unknown whether activity increases in the hippocampus, and the core network more broadly, play a causal role in episodic simulation and divergent thinking. Here we employed fMRI-guided transcranial magnetic stimulation (TMS) to assess whether temporary disruption of hippocampal brain networks impairs both episodic simulation and divergent thinking. For each of two TMS sessions, continuous θ-burst stimulation (cTBS) was applied to either a control site (vertex) or to a left angular gyrus target region. The target region was identified on the basis of a participant-specific resting-state functional connectivity analysis with a hippocampal seed region previously associated with memory, simulation, and divergent thinking. Following cTBS, participants underwent fMRI and performed a simulation, divergent thinking, and nonepisodic control task. cTBS to the target region reduced the number of episodic details produced for the simulation task and reduced idea production on divergent thinking. Performance in the control task did not statistically differ as a function of cTBS site. fMRI analyses revealed a selective and simultaneous reduction in hippocampal activity during episodic simulation and divergent thinking following cTBS to the angular gyrus versus vertex but not during the nonepisodic control task. Our findings provide evidence that hippocampal-targeted TMS can specifically modulate episodic simulation and divergent thinking, and suggest that the hippocampus is critical for these cognitive functions.

The anterior hippocampus is associated with spatial memory encoding.

There are many hypotheses regarding specialization of the anterior versus posterior hippocampus including memory encoding versus retrieval and other cognitive processes versus spatial memory. In the present functional magnetic resonance imaging study, we distinguished between the hypothesis linking encoding to the anterior hippocampus and the hypothesis linking spatial memory to the posterior hippocampus by evaluating whether spatial memory encoding involved the anterior hippocampus or the posterior hippocampus. During encoding, participants viewed abstract shapes in each of four visual field quadrants while instructed to maintain central fixation. During retrieval, old shapes were presented at fixation and participants identified the previous quadrant of each shape. A general linear model analysis did not reveal encoding activations in the anterior or posterior hippocampus. These results motivated a multi-voxel pattern analysis to assess whether there were distinct patterns of activity associated with encoding shapes in each quadrant within the anterior or posterior hippocampus. For each participant, patterns of activity associated with each quadrant were split by run (i.e., odd runs versus even runs) and the patterns in half the data were used to classify patterns in the other half of the data. Classification accuracy for items at encoding, collapsed over subsequent accuracy, was significantly above chance in the anterior but not posterior hippocampus. The present findings indicate that spatial memory encoding is associated with patterns of activity in the anterior hippocampus.

Reinstatement of Event Details during Episodic Simulation in the Hippocampus.

According to the constructive episodic simulation hypothesis, episodic simulation (i.e., imagining specific novel future episodes) draws on some of the same neurocognitive processes that support episodic memory (i.e., recalling specific past episodes). Episodic retrieval supports the ability to simulate future experiences by providing access to episodic details (e.g., the people and locations that comprise memories) that can be recombined in new ways. In the current functional neuroimaging study, we test this hypothesis by examining whether the hippocampus, a region implicated in the reinstatement of episodic information during memory, supports reinstatement of episodic information during simulation. Employing a multivoxel pattern similarity analysis, we interrogated the similarity between hippocampal neural patterns during memory and simulation at the level of individual event details. Our findings indicate that the hippocampus supports the reinstatement of detail-specific information from episodic memory during simulation, with the level of reinstatement contributing to the subjective experience of simulated details.

The core episodic simulation network dissociates as a function of subjective experience and objective content.

Episodic simulation - the mental construction of a possible future event - has been consistently associated with enhanced activity in a set of neural regions referred to as the core network. In the current functional neuroimaging study, we assessed whether members of the core network are differentially associated with the subjective experience of future events (i.e., vividness) versus the objective content comprising those events (i.e., the amount of episodic details). During scanning, participants imagined future events in response to object cues. On each trial, participants rated the subjective vividness associated with each future event. Participants completed a post-scan interview where they viewed each object cue from the scanner and verbally reported whatever they had thought about. For imagined events, we quantified the number of episodic or internal details in accordance with the Autobiographical Interview (i.e., who, what, when, and where details of each central event). To test whether core network regions are differentially associated with subjective experience or objective episodic content, imagined future events were sorted as a function of their rated vividness or the amount of episodic detail. Univariate analyses revealed that some regions of the core network were uniquely sensitive to the vividness of imagined future events, including the hippocampus (i.e., high > low vividness), whereas other regions, such as the lateral parietal cortex, were sensitive to the amount of episodic detail in the event (i.e., high > low episodic details). The present results indicate that members of the core network support distinct episodic simulation-related processes.

Adaptive constructive processes: An episodic specificity induction impacts false recall in the Deese-Roediger-McDermott paradigm.

Numerous studies indicate that an episodic specificity induction (ESI)-brief training in recollecting the details of a past experience-enhances performance on subsequent tasks that rely on episodic retrieval, including autobiographical memory, imagination, problem solving, and creative thinking. In 5 experiments, we examined whether these benefits of the ESI extend to reducing susceptibility to false memory, or whether they are accompanied by a cost in the form of increased susceptibility to false memory. To assess how ESI impacts false memory generation, we used the Deese-Roediger-McDermott (DRM) paradigm, a reliable procedure for generating false memories. When an ESI was administered after DRM list presentation and just before a free recall test, rates of false recall for critical lures were significantly enhanced relative to a control induction. These findings support the hypothesis that ESI operates to boost recollection of illusory episodic details associated with critical lures in the DRM, and suggest that constructive rather than reproductive episodic retrieval processes support the wide-ranging effects of ESI on a range of cognitive tasks. (PsycINFO Database Record (c) 2019 APA, all rights reserved).