Metacognitive Awareness and the Subjective Experience of Remembering in Aphantasia.

Individuals with aphantasia, a nonclinical condition typically characterized by mental imagery deficits, often report reduced episodic memory. However, findings have hitherto rested largely on subjective self-reports, with few studies experimentally investigating both objective and subjective aspects of episodic memory in aphantasia. In this study, we tested both aspects of remembering in aphantasic individuals using a custom 3-D object and spatial memory task that manipulated visuospatial perspective, which is considered to be a key factor determining the subjective experience of remembering. Objective and subjective measures of memory performance were taken for both object and spatial memory features under different perspective conditions. Surprisingly, aphantasic participants were found to be unimpaired on all objective memory measures, including those for object memory features, despite reporting weaker overall mental imagery experience and lower subjective vividness ratings on the memory task. These results add to newly emerging evidence that aphantasia is a heterogenous condition, where some aphantasic individuals may lack metacognitive awareness of mental imagery rather than mental imagery itself. In addition, we found that both participant groups remembered object memory features with greater precision when encoded and retrieved in the first person versus third person, suggesting a first-person perspective might facilitate subjective memory reliving by enhancing the representational quality of scene contents.

Demands on perceptual and mnemonic fidelity are a key determinant of age-related cognitive decline throughout the lifespan.

Aging results in less detailed memories, reflecting reduced fidelity of remembered compared to real-world representations. We tested whether poorer representational fidelity across perception, short-term memory (STM), and long-term memory (LTM) are among the earliest signs of cognitive aging. Our paradigm probed target-lure object mnemonic discrimination and precision of object-location binding. Across the lifespan, cognitive deficits were observed in midlife when detailed stimulus representations were required for perceptual and short/long-term forced choice mnemonic discrimination. A continuous metric of object-location source memory combined with computational modeling demonstrated that errors in STM and LTM in middle-aged adults were largely driven by a loss of precision for retrieved memories, not necessarily by forgetting. On a trial-by-trial basis, fidelity of item and spatial information was more tightly bound in LTM compared to STM with this association being unaffected by age. Standard neuropsychological tests without demands on memory quality (digit span, verbal learning) were less sensitive to age effects than STM and LTM precision. Perceptual discrimination predicted mnemonic discrimination. Neuropsychological proxies for prefrontal executive functions correlated with STM, but not LTM fidelity. Conversely, neuropsychological indicators of hippocampal integrity correlated with mnemonic discrimination and precision of both STM and LTM, suggesting partially dissociable mechanisms of interindividual variability in STM and LTM fidelity. These findings suggest that reduced representational fidelity is a hallmark of cognitive aging across perception, STM, and LTM and can be observed from midlife onward. Continuous memory precision tasks may be promising for the early detection of subtle age-related cognitive decline. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

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.

Medial temporal lobe structure, mnemonic and perceptual discrimination in healthy older adults and those at risk for mild cognitive impairment.

Cognitive tests sensitive to the integrity of the medial temporal lobe (MTL), such as mnemonic discrimination of perceptually similar stimuli, may be useful early markers of risk for cognitive decline in older populations. Perceptual discrimination of stimuli with overlapping features also relies on MTL but remains relatively unexplored in this context. We assessed mnemonic discrimination in two test formats (Forced Choice, Yes/No) and perceptual discrimination of objects and scenes in 111 community-dwelling older adults at different risk status for cognitive impairment based on neuropsychological screening. We also investigated associations between performance and MTL sub-region volume and thickness. The at-risk group exhibited reduced entorhinal thickness and impaired perceptual and mnemonic discrimination. Perceptual discrimination impairment partially explained group differences in mnemonic discrimination and correlated with entorhinal thickness. Executive dysfunction accounted for Yes/No deficits in at-risk adults, demonstrating the importance of test format for the interpretation of memory decline. These results suggest that perceptual discrimination tasks may be useful tools for detecting incipient cognitive impairment related to reduced MTL integrity in nonclinical populations.

The devil may be in the details: The need for contextually rich stimuli in memory consolidation research.

Systems consolidation theory (SCT) proposes that the hippocampus is not required for retrieval of remote memories. In this issue, Tallman and colleagues observe reduced hippocampal-cortical connectivity in recognition memory as a function of memory age, which they interpret as supportive of SCT. We suggest that research seeking to inform this debate would benefit from using perceptually rich stimuli that promote the recollection of high-fidelity contextual details. Tests of recognition alone may not be capable of discerning whether reductions in hippocampal activity or connectivity reflect remote memory retrieval independent of hippocampus (consistent with SCT) or a time-dependent decline in episodic detail.

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.

I remember it like it was yesterday: Age-related differences in the subjective experience of remembering.

It has been frequently described that older adults subjectively report the vividness of their memories as being as high, or even higher, than young adults, despite poorer objective memory performance. Here, we review studies that examined age-related differences in the subjective experience of memory vividness. By examining vividness calibration and resolution, studies using different types of approaches converge to suggest that older adults overestimate the intensity of their vividness ratings relative to young adults, and that they rely on retrieved memory details to a lesser extent to judge vividness. We discuss potential mechanisms underlying these observations. Inflation of memory vividness with regard to the richness of memory content may stem from age-differences in vividness criterion or scale interpretation and psycho-social factors. The reduced reliance on episodic memory details in older adults may stem from age-related differences in how they monitor these details to make their vividness ratings. Considered together, these findings emphasize the importance of examining age-differences in memory vividness using different analytical methods and they provide valuable evidence that the subjective experience of remembering is more than the reactivation of memory content. In this vein, we recommend that future studies explore the links between memory vividness and other subjective memory scales (e.g., ratings of details or memory confidence) in healthy aging and/or other populations, as it could be used as a window to better characterize the cognitive processes that underpin the subjective assessment of the quality of recollected events.

Brain Mechanisms Underlying the Subjective Experience of Remembering.

The ability to remember events in vivid, multisensory detail is a significant part of human experience, allowing us to relive previous encounters and providing us with the store of memories that shape our identity. Recent research has sought to understand the subjective experience of remembering, that is, what it feels like to have a memory. Such remembering involves reactivating sensory-perceptual features of an event and the thoughts and feelings we had when the event occurred, integrating them into a conscious first-person experience. It allows us to reflect on the content of our memories and to understand and make judgments about them, such as distinguishing events that actually occurred from those we might have imagined or been told about. In this review, we consider recent evidence from functional neuroimaging in healthy participants and studies of neurological and psychiatric conditions, which is shedding new light on how we subjectively experience remembering.

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.

Memory precision of object-location binding is unimpaired in APOE ε4-carriers with spatial navigation deficits.

Research suggests that tests of memory fidelity, feature binding and spatial navigation are promising for early detection of subtle behavioural changes related to Alzheimer's disease. In the absence of longitudinal data, one way of testing the early detection potential of cognitive tasks is through the comparison of individuals at different genetic risk for Alzheimer's dementia. Most studies have done so using samples aged 70 years or older. Here, we tested whether memory fidelity of long-term object-location binding may be a sensitive marker even among cognitively healthy individuals in their mid-60s by comparing participants at low and higher risk based on presence of the ε4-allele of the apolipoprotein gene (n = 26 ε3ε3, n = 20 ε3ε4 carriers). We used a continuous report paradigm in a visual memory task that required participants to recreate the spatial position of objects in a scene. We employed mixture modelling to estimate the two distinct memory processes that underpin the trial-by-trial variation in localization errors: retrieval success which indexes the proportion of trials where participants recalled any information about an object's position and the precision with which participants retrieved this information. Prior work has shown that these memory paradigms that separate retrieval success from precision are capable of detecting subtle differences in mnemonic fidelity even when retrieval success could not. Nonetheless, Bayesian analyses found good evidence that ε3ε4 carriers did not remember fewer object locations [F(1, 42) = 0.450, P = 0.506, BF01 = 3.02], nor was their precision for the spatial position of objects reduced compared to ε3ε3 carriers [F(1, 42) = 0.12, P = 0.726, BF01 = 3.19]. Because the participants in the sample presented here were a subset of a study on apolipoprotein ε4-carrier status and spatial navigation in the Sea Hero Quest game [Coughlan et al., 2019. PNAS, 116(9)], we obtained these data to contrast genetic effects on the two tasks within the same sample (n = 33). Despite the smaller sample size, wayfinding deficits among ε3ε4 carriers could be replicated [F(1, 33) = 5.60, P = 0.024, BF10 = 3.44]. Object-location memory metrics and spatial navigation scores were not correlated (all r < 0.25, P > 0.1, 0 < BF10 < 3). These findings show spared object-location binding in the presence of a detrimental apolipoprotein ε4 effect on spatial navigation. This suggests that the sensitivity of memory fidelity and binding tasks may not extend to individuals with one ε4-allele in their early to mid-60s. The results provide further support to prior proposals that spatial navigation may be a sensitive marker for the earliest cognitive changes in Alzheimer's disease, even before episodic memory.

A Unifying Account of Angular Gyrus Contributions to Episodic and Semantic Cognition.

The angular gyrus (AG) region of lateral parietal cortex has been implicated in a wide variety of tasks and functions, generating numerous influential theories. However, these theories largely fail to explain why so many apparently distinct cognitive activities implicate common parietal structures. We propose a unifying model, based on a set of central principles, to account for coalescences of cognitive task activations across AG. To illustrate the proposed framework, we show how these principles account for findings from studies of episodic and semantic memory that have independently implicated the same AG regions but thus far been considered from largely domain-specific perspectives. We conclude that AG computations, as part of a wider lateral parietal system, enable the online dynamic buffering of multisensory spatiotemporally extended representations.

Executive function and high ambiguity perceptual discrimination contribute to individual differences in mnemonic discrimination in older adults.

Mnemonic discrimination deficits, or impaired ability to discriminate between similar events in memory, is a hallmark of cognitive aging, characterised by a stark age-related increase in false recognition. While individual differences in mnemonic discrimination have gained attention due to potential relevance for early detection of Alzheimer's disease, our understanding of the component processes that contribute to variability in task performance across older adults remains limited. The present investigation explores the roles of representational quality, indexed by perceptual discrimination of objects and scenes with overlapping features, and strategic retrieval ability, indexed by standardised tests of executive function, to mnemonic discrimination in a large cohort of older adults (N=124). We took an individual differences approach and characterised the contributions of these factors to performance under Forced Choice (FC) and Yes/No (YN) recognition memory formats, which place different demands on strategic retrieval. Performance in both test formats declined with age. Accounting for age, individual differences in FC memory performance were best explained by perceptual discrimination score, whereas YN memory performance was best explained by executive functions. A linear mixed model and dominance analyses confirmed the relatively greater importance of perceptual discrimination over executive functioning for FC performance, while the opposite was true for YN. These findings highlight parallels between perceptual and mnemonic discrimination in aging, the importance of considering demands on executive functions in the context of mnemonic discrimination, and the relevance of test format for modulating the impact of these factors on performance in older adults.

Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia.

All perception is a construction of the brain from sensory input. Our first perceptions begin during gestation, making fetal brain development fundamental to how we experience a diverse world. Hallucinations are percepts without origin in physical reality that occur in health and disease. Despite longstanding research on the brain structures supporting hallucinations and on perinatal contributions to the pathophysiology of schizophrenia, what links these two distinct lines of research remains unclear. Sulcal patterns derived from structural magnetic resonance (MR) images can provide a proxy in adulthood for early brain development. We studied two independent datasets of patients with schizophrenia who underwent clinical assessment and 3T MR imaging from the United Kingdom and Shanghai, China (n = 181 combined) and 63 healthy controls from Shanghai. Participants were stratified into those with (n = 79 UK; n = 22 Shanghai) and without (n = 43 UK; n = 37 Shanghai) hallucinations from the PANSS P3 scores for hallucinatory behaviour. We quantified the length, depth, and asymmetry indices of the paracingulate and superior temporal sulci (PCS, STS), which have previously been associated with hallucinations in schizophrenia, and constructed cortical folding covariance matrices organized by large-scale functional networks. In both ethnic groups, we demonstrated a significantly shorter left PCS in patients with hallucinations compared to those without, and to healthy controls. Reduced PCS length and STS depth corresponded to focal deviations in their geometry and to significantly increased covariance within and between areas of the salience and auditory networks. The discovery of neurodevelopmental alterations contributing to hallucinations establishes testable models for these enigmatic, sometimes highly distressing, perceptions and provides mechanistic insight into the pathological consequences of prenatal origins.

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).

Neural evidence for age-related differences in representational quality and strategic retrieval processes.

Mounting behavioral evidence suggests that declines in both representational quality and controlled retrieval processes contribute to episodic memory decline with age. The present study sought neural evidence for age-related change in these factors by measuring neural differentiation during encoding of paired associates and changes in regional blood oxygenation level-dependent activity and functional connectivity during retrieval conditions that placed low (intact pairs) and high (recombined pairs) demands on controlled retrieval processes. Pattern similarity analysis revealed age-related declines in the differentiation of stimulus representations at encoding, manifesting as both reduced pattern similarity between closely related events and increased pattern similarity between distinct events. During retrieval, both groups increased recruitment of areas within the core recollection network when endorsing studied pairs, including the hippocampus and angular gyrus. In contrast, only younger adults increased recruitment of, and hippocampal connectivity with, lateral prefrontal regions during correct rejections of recombined pairs. These results provide evidence for age-related changes in representational quality and in the neural mechanisms supporting memory retrieval under conditions of high, but not low, control demand.

Meta-analytic Evidence for the Plurality of Mechanisms in Transdiagnostic Structural MRI Studies of Hallucination Status.

BACKGROUND: Hallucinations are transmodal and transdiagnostic phenomena, occurring across sensory modalities and presenting in psychiatric, neurodegenerative, neurological, and non-clinical populations. Despite their cross-category occurrence, little empirical work has directly compared between-group neural correlates of hallucinations. METHODS: We performed whole-brain voxelwise meta-analyses of hallucination status across diagnoses using anisotropic effect-size seed-based d mapping (AES-SDM), and conducted a comprehensive systematic review in PubMed and Web of Science until May 2018 on other structural correlates of hallucinations, including cortical thickness and gyrification. FINDINGS: 3214 abstracts were identified. Patients with psychiatric disorders and hallucinations (eight studies) exhibited reduced gray matter (GM) in the left insula, right inferior frontal gyrus, left anterior cingulate/paracingulate gyrus, left middle temporal gyrus, and increased in the bilateral fusiform gyrus, while patients with neurodegenerative disorders with hallucinations (eight studies) showed GM decreases in the left lingual gyrus, right supramarginal gyrus/parietal operculum, left parahippocampal gyrus, left fusiform gyrus, right thalamus, and right lateral occipital gyrus. Group differences between psychiatric and neurodegenerative hallucination meta-analyses were formally confirmed using Monte Carlo randomizations to determine statistical significance, and a jackknife sensitivity analysis established the reproducibility of results across nearly all study combinations. For other structural measures (28 studies), the most consistent findings associated with hallucination status were reduced cortical thickness in temporal gyri in schizophrenia and altered hippocampal volume in Parkinson's disease and dementia. Additionally, increased severity of hallucinations in schizophrenia correlated with GM reductions within the left superior temporal gyrus, right middle temporal gyrus, bilateral supramarginal and angular gyri. INTERPRETATION: Distinct patterns of neuroanatomical alteration characterize hallucination status in patients with psychiatric and neurodegenerative diseases, suggesting a plurality of anatomical signatures. This approach has implications for treatment, theoretical frameworks, and generates refutable predictions for hallucinations in other diseases and their occurrence within the general population. FUNDING: None.

Multimodal Integration and Vividness in the Angular Gyrus During Episodic Encoding and Retrieval.

Much evidence suggests that the angular gyrus (AnG) is involved in episodic memory, but its precise role has yet to be determined. We examined two possible accounts within the same experimental paradigm: the "cortical binding of relational activity" (CoBRA) account (Shimamura, 2011), which suggests that the AnG acts as a convergence zone that binds multimodal episodic features, and the subjectivity account (Yazar et al., 2012), which implicates AnG involvement in subjective mnemonic experience (such as vividness or confidence). fMRI was used during both encoding and retrieval of paired associates. During study, female and male human participants memorized picture-pairs of common objects (in the unimodal task) or of an object-picture and an environmental sound (in the crossmodal task). At test, they performed a cued-recall task and further indicated the vividness of their memory. During retrieval, BOLD activation in the AnG was greatest for vividly remembered associates, consistent with the subjectivity account. During encoding, the same effect of vividness was found, but this was further modulated by task: greater activations were associated with subsequent recall in the crossmodal than the unimodal task. Therefore, encoding data suggest an additional role to the AnG in crossmodal integration, consistent with its role at retrieval proposed by CoBRA. These results resolve some of the puzzles in the literature and indicate that the AnG can play different roles during encoding and retrieval as determined by the cognitive demands posed by different mnemonic tasks.SIGNIFICANCE STATEMENT We offer new insights into the multiplicity of processes that are associated with angular gyrus (AnG) activation during encoding and retrieval of newly formed memories. We used fMRI while human participants learned and subsequently recalled pairs of objects presented to the same sensory modality or to different modalities. We were able to show that the AnG is involved when vivid memories are created and retrieved, as well as when encoded information is integrated across different sensory modalities. These findings provide novel evidence for the contribution of the AnG to our subjective experience of remembering alongside its role in integrative processes that promote subsequent memory.

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.

Exploring the neurocognitive basis of episodic recollection in autism.

Increasing evidence indicates that the subjective experience of recollection is diminished in autism spectrum disorder (ASD) compared to neurotypical individuals. The neurocognitive basis of this difference in how past events are re-experienced has been debated and various theoretical accounts have been proposed to date. Although each existing theory may capture particular features of memory in ASD, recent research questions whether any of these explanations are alone sufficient or indeed fully supported. This review first briefly considers the cognitive neuroscience of how episodic recollection operates in the neurotypical population, informing predictions about the encoding and retrieval mechanisms that might function atypically in ASD. We then review existing research on recollection in ASD, which has often not distinguished between different theoretical explanations. Recent evidence suggests a distinct difficulty engaging recollective retrieval processes, specifically the ability to consciously reconstruct and monitor a past experience, which is likely underpinned by altered functional interactions between neurocognitive systems rather than brain region-specific or process-specific dysfunction. This integrative approach serves to highlight how memory research in ASD may enhance our understanding of memory processes and networks in the typical brain. We make suggestions for future research that are important for further specifying the neurocognitive basis of episodic recollection in ASD and linking such difficulties to social developmental and educational outcomes.