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Simons, J. S.

Publications and source records attributed to Simons, J. S..

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Age-related differences in episodic memory precision are robust across time of day, chronotype, and testing format

Older adults typically exhibit reduced episodic memory precision, while maintaining relatively preserved retrieval success. However, little is known about whether these age-related differences are influenced by internal biological factors (e.g., chronotype) or external testing conditions (e.g., experiment format, time of day). To address this question, younger and older adults completed an object-location memory task online, either in the morning or evening, and either with or without video-based supervision. Memory performance was assessed using mean absolute error and Bayesian hierarchical mixture modelling, which dissociated memory precision ({kappa}) from the probability of memory-based responding ({theta}). Immediate memory performance was high across age groups, irrespective of time of day. Greater encoding error predicted greater retrieval error, and participants tested in the video condition exhibited lower recall error and higher recognition performance than those tested without supervision. Consistent with prior studies, older adults exhibited reduced memory precision relative to younger adults, whereas retrieval success remained largely intact. However, Bayesian Hierarchical Modelling provided no evidence that time of day, experiment format, or their interactions with age influenced either memory precision or retrieval probability. Older adults reported stronger morning preferences than younger adults, and participants generally selected testing times that aligned with their chronotype. Nevertheless, alignment between chronotype and testing time did not modulate memory performance. The results indicate that age-related differences in episodic memory precision are robust across variations in testing context, including time of day, experiment format, and individual differences in chronotype. More broadly, the results support the feasibility of remote and unsupervised testing for memory precision research and suggest that chronotype and testing time are unlikely to be major sources of variability in immediate object-location memory performance.

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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, 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 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 angular gyrus. Grey matter volume of the angular gyrus 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 angular gyrus in constraining the fidelity of episodic remembering in older age, yielding new insights into parietal contributions to age-related episodic memory decline.

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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 subregion 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 non-clinical populations.

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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 (Johnson & Raye, 1981). 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: agency decisions that distinguish actions performed by participants and the experimenter, and perceptual decisions that distinguish perceived and imagined experiences. The data revealed memory precision to be associated with higher accuracy in both agency and perceptual reality monitoring decisions, with reduced 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, 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. Angular gyrus may, therefore, be important for the ability to imbue remembered experiences with a sense of self-agency, a key component of autonoetic consciousness that characterises episodic memory (Tulving, 1985).

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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 Alzheimers disease (AD). 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 AD. 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 {varepsilon}4-allele of the apolipoprotein gene (n=26 {varepsilon}3{varepsilon}3, n=20 {varepsilon}3{varepsilon}4 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 localisation errors: retrieval success which indexes the proportion of trials where participants recalled any information about an objects 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, a Bayesian analysis found good evidence that {varepsilon}3{varepsilon}4 carriers did not remember fewer object locations (F(1, 42)=.450, p=.506, BF01 =3.02), nor was their precision for the spatial position of objects reduced compared to {varepsilon}3{varepsilon}3 carriers (F(1, 42)=.12, p=.726, BF01 =3.19). Because the participants in the sample presented here were a subset of a study on APOE effects on spatial navigation in the Sea Hero Quest game (Coughlan et al., 2019. PNAS, 116(9)), we obtained these data to contrast APOE effects on the two tasks within the same sample (n=33). Despite the smaller sample size, wayfinding deficits among {varepsilon}3{varepsilon}4 could be replicated (F(1, 33) =5.60, p=.024, BF10 =3.44). Object-location memory metrics and spatial navigation scores were not correlated (all r<.25, p>.1, 0<BF10 <3). These findings show spared object-location binding in the presence of a detrimental APOE {varepsilon}4 effect on spatial navigation. This suggests that the sensitivity of memory fidelity and binding tasks may not extend to individuals with one {varepsilon}4-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 AD-dependent cognitive changes, even before episodic memory.

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Hippocampal-cortical encoding activity predicts the precision of episodic memory

Our recollections of past experiences can vary both in 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 behavioural 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 identify a hippocampal-cortical encoding basis for episodic memory precision, and suggest a contribution of shared cortical encoding mechanisms to the formation of both accessible and precise memory representations.

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Encoding Variability: When Pattern Reactivation Does Not Benefit Context Memory

A growing body of evidence suggests that neural pattern reactivation supports successful memory formation across multiple study episodes. Previous studies investigating the beneficial effects of repeated encoding typically presented the same stimuli repeatedly under the same encoding task instructions. In contrast, repeating stimuli in different contexts is associated with superior item memory, but poorer memory for contextual features varying across repetitions. In the present functional magnetic-resonance imaging (fMRI) study, we predicted dissociable mechanisms to underlie the successful formation of context memory when the context in which stimuli are repeated is either held constant or varies at each stimulus presentation. Twenty participants studied names of famous people four times, either in the same task repeatedly, or in four different encoding tasks. This was followed by a surprise recognition memory test, including a source judgement about the encoding task. Behaviourally, different task encoding compared to same task encoding was associated with fewer correct context memory judgements but also better item memory, as reflected in fewer misses. Searchlight representational similarity analysis revealed fMRI pattern reactivation in the posterior cingulate cortex to be higher for correct compared to incorrect source memory judgements in the same task condition, with the opposite pattern being observed in the different task condition. It was concluded that higher levels of pattern reactivation in the posterior cingulate cortex index generalisation across context information, which in turn may improve item memory performance during encoding variability but at the cost of contextual features.

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Meta-analytic evidence for the plurality of mechanisms in transdiagnostic structural MRI studies of hallucination status

BACKGROUNDHallucinations 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.\n\nMETHODSWe performed whole-brain voxelwise meta-analyses of hallucination status across diagnoses using 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.\n\nFINDINGS3214 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 meta-analyses were formally confirmed and a jackknife sensitivity analysis established the reproducibility of results across nearly all study combinations. For other 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 Parkinsons disease and dementia.\n\nINTERPRETATIONDistinct 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.\n\nFUNDINGNone.\n\nResearch in contextO_ST_ABSEvidence before this studyC_ST_ABSThere is increasing recognition that hallucinations occur beyond the archetype of schizophrenia, presenting in other psychiatric disorders, neurological and neurodegenerative conditions, and among the general population. Not only are hallucinations a transdiagnostic phenomenon, but also the experience of hallucinating is phenomenologically diverse, varying in modality, content, frequency, and affect. It has been suggested that no one type of hallucination is pathognomic to any one disorder, but rather that hallucinations may exist on a continuum. However, limited research has been done to directly compare the underlying neuroanatomy of hallucinations between different disorders. With this aim, we conducted a meta-analysis and systematic review of structural MRI studies comparing individuals who experience hallucinations with those who do not, to investigate the brain morphology related to the transdiagnostic presentation of hallucinations. We searched PubMed and Web of Science with no start date limit, up to May 2018 using the keyword combination (hallucinat*) AND (MRI OR magnetic resonance imaging OR morphology OR voxel?based OR morphometr* OR neural correlate OR structur*). We included only studies with a within-group no-hallucination control to tease out structural changes specific to hallucinations from effects of the broader pathology. Neuroimaging meta-analyses were conducted on studies performing whole-brain voxelwise gray matter differences, while studies assessing other structural correlates were qualitatively synthesized.\n\nAdded value of this studyThis is the first meta-analysis to illustrate the brain structural correlates of hallucination occurrence derived from T1-weighted MRI, and to do so in a comparative manner across clinical groups. We identified two distinct gray matter substrates for hallucination presence in psychiatric compared to neurodegenerative diseases, which we hypothesise constitute at least two distinct mechanisms. In addition, we qualitatively assessed other structural neuroimaging studies over a variety of morphometric indices. We therefore provide a complete characterization of current knowledge of the brain morphology associated with hallucinations across clinical status and modality.\n\nImplications of all the available evidenceOur findings show at least two structural substrates that link to the hallucinatory experience. This informs theoretical work on hallucinations which have to date been limited in generating unifying direction-specific predictions of brain structure and function. Understanding the plurality of anatomical signatures of hallucinations may also inform treatment strategies. We predict that other disorders in which patients experience hallucinations can be categorised by our approach based on the broader phenotype; for example, hallucinations in personality disorder may be of the psychiatric type, and similarly for early onset hallucinations in the general population, whilst later onset will be neurodegenerative. Moreover, by differentiating the mechanisms of hallucinations we recommend the contextualising of research by the appropriate phenotype.

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Alpha Oscillations During Incidental Encoding Predict Subsequent Memory For New "Foil" Information

People can employ adaptive strategies to increase the likelihood that previously encoded information will be successfully retrieved. One such strategy is to constrain retrieval towards relevant information by re-implementing the neurocognitive processes that were engaged during encoding. Using electroencephalography (EEG), we examined the temporal dynamics with which constraining retrieval towards semantic versus non-semantic information affects the processing of new \"foil\" information encountered during a memory test. Time-frequency analysis of EEG data acquired during an initial study phase revealed that semantic compared to non-semantic processing was associated with alpha decreases in a left frontal electrode cluster from around 600ms after stimulus onset. Successful encoding of semantic versus non-semantic foils during a subsequent memory test was related to decreases in alpha oscillatory activity in the same left frontal electrode cluster, which emerged relatively late in the trial at around 1000-1600ms after stimulus onset. Across subjects, left frontal alpha power elicited by semantic processing during the study phase correlated significantly with left frontal alpha power associated with semantic foil encoding during the memory test. Furthermore, larger left frontal alpha power decreases elicited by semantic foil encoding during the memory test predicted better subsequent semantic foil recognition in an additional surprise foil memory test. These findings indicate that constraining retrieval towards semantic information involves re-implementing semantic encoding operations that are mediated by alpha oscillations, and that such re-implementation occurs at a late stage of memory retrieval perhaps reflecting additional monitoring processes.

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