Investigating the neural basis of schematic false memories by examining schematic and lure pattern similarity.

ABSTRACTSchemas allow us to make assumptions about the world based upon previous experiences and aid in memory organisation and retrieval. However, a reliance on schemas may also result in increased false memories to schematically related lures. Prior neuroimaging work has linked schematic processing in memory tasks to activity in prefrontal, visual, and temporal regions. Yet, it is unclear what type of processing in these regions underlies memory errors. The current study examined where schematic lures exhibit greater neural similarity to schematic targets, leading to this memory error, as compared to neural overlap with non-schematic lures, which, like schematic lures, are novel items at retrieval. Results showed that patterns of neural activity in ventromedial prefrontal cortex, medial frontal gyrus, middle temporal gyrus, hippocampus, and occipital cortices exhibited greater neural pattern similarity for schematic targets and schematic lures than between schematic lures and non-schematic lures. As such, results suggest that schematic membership, and not object history, may be more critical to the neural processes underlying memory retrieval in the context of a strong schema.

Examining the neural basis of unitization: A review.

Associative memory refers to the ability to form and remember associations between individual pieces of information rather than memory for a single object or word. Encoding associations in memory tends to be a more difficult task than item (only) encoding, because associative memory requires encoding multiple items as well as the specific links amongst the items. Accordingly, researchers have worked to identify interventions and strategies to reduce the effort and neural resources required for successful associative memory processing. Unitization is one such strategy that has traditionally been defined as the process by which two or more discrete items are processed, or encoded, such that they are perceived as a single ensemble. The current review explores the neural research on unitization while considering the behavioral benefits that accompany the process.

Investigating the neural basis of schematic false memories by examining schematic and lure pattern similarity.

Schemas allow us to make assumptions about the world based upon previous experiences and aid in memory organization and retrieval. However, a reliance on schemas may also result in increased false memories to schematically related lures. Prior neuroimaging work has linked schematic processing in memory tasks to activity in prefrontal, visual, and temporal regions. Yet, it is unclear what type of processing in these regions underlies memory errors. The current study examined where schematic lures exhibit greater neural similarity to schematic targets, leading to this memory error, as compared to neural overlap with non-schematic lures, which, like schematic lures, are novel items at retrieval. Results showed that patterns of neural activity in ventromedial prefrontal cortex, medial frontal gyrus, middle temporal gyrus, hippocampus, and occipital cortices exhibited greater neural pattern similarity for schematic targets and schematic lures than between schematic lures and non-schematic lures. As such, results suggest that schematic membership, and not object history, may be more critical to the neural processes underlying memory retrieval in the context of a strong schema.

Memory and creativity: A meta-analytic examination of the relationship between memory systems and creative cognition.

Increasing evidence suggests that specific memory systems (e.g., semantic vs. episodic) may support specific creative thought processes. However, there are a number of inconsistencies in the literature regarding the strength, direction, and influence of different memory (semantic, episodic, working, and short-term) and creativity (divergent and convergent thinking) types, as well as the influence of external factors (age, stimuli modality) on this purported relationship. In this meta-analysis, we examined 525 correlations from 79 published studies and unpublished datasets, representing data from 12,846 individual participants. We found a small but significant (r = .19) correlation between memory and creative cognition. Among semantic, episodic, working, and short-term memory, all correlations were significant, but semantic memory - particularly verbal fluency, the ability to strategically retrieve information from long-term memory - was found to drive this relationship. Further, working memory capacity was found to be more strongly related to convergent than divergent creative thinking. We also found that within visual creativity, the relationship with visual memory was greater than that of verbal memory, but within verbal creativity, the relationship with verbal memory was greater than that of visual memory. Finally, the memory-creativity correlation was larger for children compared to young adults despite no impact of age on the overall effect size. These results yield three key conclusions: (1) semantic memory supports both verbal and nonverbal creative thinking, (2) working memory supports convergent creative thinking, and (3) the cognitive control of memory is central to performance on creative thinking tasks.

Does unitization really function like items? The role of interference on item and associative memory processes.

Associative memory declines as we age, while item memory remains relatively stable. Previous work has shown that, in both younger and older adults, while item recognition declines linearly across time and interference, associative recognition declines only with longer delays and more interference. Unitization is a memory process found to support associative memory by allowing pairs to presumably be processed like single items. Research has found that unitization can benefit memory in aging by boosting associative memory to be on par with that of younger adults. Yet it remains unclear exactly the mechanism responsible for this enhancement in memory. The current studies aimed to determine whether unitized pairs show similar memory to that of items or associations with increasing time and interference, and determine how physically similar unitized pairs must be to perform like items and examine the effect of age on unitization in a continuous recognition paradigm. The results show that while unitized pairs exhibit higher corrected recognition compared with associative pairs at all lags, unitized pairs are not remembered to the degree that items are. It is critical that unitization boosts accurate recognition of pairs in both age groups across all early and middle lags compared with associative pairs. The results suggest that unitization may promote a more efficient associative link than unrelated associations over increasing time and interference, but the benefit does not reach that of item memory. These results demonstrate that while unitization benefits corrected recognition with earlier interference, its effect may not hold with later interference.

Age-related differences in encoding-retrieval similarity and their relationship to false memory.

Typical aging is associated with increases in false memory rates among older adults. Such errors are frequently associated with differential neural activity during encoding and retrieval in older compared to younger adults within visual cortices and the hippocampus. It remains unknown how pattern similarity reductions relate to false memories in healthy aging. Using encoding-retrieval similarity (ERS) analyses in a sample of younger and older adults, we examined how the similarity of neural patterns between memory phases associated with target and lure objects was impacted by age and contributed to false memory rates. Single-item ERS for targets and lures was reduced by age throughout much of the ventral visual stream and the posterior hippocampus. Furthermore, ERS associated with perceptual lures within the visual stream maintained differential relationships with false memory. Finally, a global ERS metric accounted for age deficits in single-item ERS, but did not contribute to false memory rates. These findings highlight the contribution of age-related reductions in ERS across multiple representational levels to false memories in healthy aging.

Understanding associative false memories in aging using multivariate analyses.

Age-related declines in associative memory are ubiquitous, with decreases in behavioral discriminability largely arising from increases in false memories for recombined lures. Using representational similarity analyses to examine the neural basis of associative false memories in aging, the current study found that neural pattern similarity between Hits and FAs and Hits and CRs differed as a function of age in occipital ROIs, such that older adults exhibited a smaller difference between the two similarity metrics than did younger adults. Additionally, greater Hit-FA representational similarity correlated with increases in associative FAs across several ROIs. Results suggest that while neural representations underlying targets may not differ across ages, greater pattern similarity between the neural representation of targets and lures may reflect reduced distinctiveness of the information encoded in memory, such that old and new items are more difficult to discriminate, leading to more false alarms.

The effect of memory cue duration on performance in the directed forgetting task in healthy aging.

Although forgetting is usually considered a memory error, intentional forgetting can function as an adaptive mechanism. The current study examined the effect of increased processing time on directed forgetting in aging as a mechanism to compensate for age-related forgetting. Specifically, an item-method directed forgetting paradigm was used in conjunction with Remember/Know/New responding to examine the effect of cue duration (1, 3, 5 s) on directed forgetting and remembering in younger and older adults. Results indicated that increased processing time improved performance in both age groups. Critically, older adults exhibited a linear increase in directed remembering performance across all cue durations which was related to individual differences in cognitive reserve. Specifically, those older adults with the highest levels of cognitive functioning showed the greatest memory benefit in the longest cue duration condition. These findings indicate the importance of processing time in accounting for intentional memory performance in older adults.

The influence of item familiarization on neural discriminability during associative memory encoding and retrieval.

Associative memory requires one to encode and form memory representations not just for individual items, but for the association or link between those items. Past work has suggested that associative memory is facilitated when individual items are familiar rather than simultaneously learning the items and their associative link. The current study employed multivoxel pattern analyses (MVPA) to investigate whether item familiarization prior to associative encoding affects the distinctiveness of neural patterns, and whether that distinctiveness is also present during associative retrieval. Our results suggest that prior exposure to item stimuli impacts the representations of their shared association compared to stimuli that are novel at the time of associative encoding throughout most of the associative memory network. While this distinction was also present at retrieval, the overall extent of the difference was diminished. Overall the results suggest that stimulus familiarity influences the representation of associative pairings during memory encoding and retrieval, and the pair-specific representation is maintained across memory phases irrespective of this distinction.

Fornix white matter microstructure differentially predicts false recollection rates in older and younger adults.

Healthy aging is accompanied by increased false remembering in addition to reduced successful remembering in older adults. Neuroimaging studies implicate age-related differences in the involvement of medial temporal lobe and fronto-parietal regions in mediating highly confident false recollection. However, no studies have directly examined the relationship between white matter microstructure and false recollection in younger and older adults. Using diffusion-weighted imaging and probabilistic tractography, we examined how white matter microstructure within tracts connecting the hippocampus and the fronto-parietal retrieval network contribute to false recollection rates in healthy younger and older adults. We found only white matter microstructure within the fornix contributed to false recollection rates, and this relationship was specific to older adults. Fornix white matter microstructure did not contribute to true recollection rate, nor did common white matter contribute to false recollection, suggesting fornix microstructure is explicitly associated with highly confident false memories in our sample of older adults. These findings underlie the importance of examining microstructural correlates associated with false recollection in younger and older adults.

Cross-situational statistical learning in younger and older adults.

Research investigating statistical learning, the process of tracking regularities in the environment, in older adults has been limited; with existing studies suggesting there are age-related declines. We aim to further understand older adults' statistical learning abilities using a cross-situational statistical learning paradigm in which learners map novel words to novel objects. In Experiment 1, we manipulated task difficulty and found an overall age deficit but no interaction between age and difficulty. In Experiment 2, after extended practice with a first set of object-word mappings, learners could remap a subset of previously learned words to novel objects. Based on hyper-binding, older adults might be more willing to remap previously learned words to novel objects. However, despite overall poorer learning, older adults were actually less likely to remap. Even though older adults may have an associative memory deficit, learned associations are not more weakly bound for older relative to younger adults.

Examining the Neural Basis of Congruent and Incongruent Configural Contexts during Associative Retrieval.

Disrupting the configural context, or relative organization and orientation of paired stimuli, between encoding and retrieval negatively impacts memory. Using univariate and multivariate fMRI analyses, we examined the effect of retaining and manipulating the configural context on neural mechanisms supporting associative retrieval. Behavioral results showed participants had significantly higher hit rates for recollecting pairs in a contextually congruent, versus incongruent, configuration. In addition, contextual congruency between memory phases was a critical determinant to characterizing both the magnitude and patterns of neural activation within visual and parietal cortices. Regions within visual cortices also exhibited higher correlations between patterns of activity at encoding and retrieval when configural context was congruent across memory phases than incongruent. Collectively, these findings shed light on how manipulating configural context between encoding and retrieval affects associative recognition, with changes in the configural context leading to reductions in information transfer and increases in task difficulty.

Lexical frequency affects functional activation and accuracy in picture naming among older and younger adults.

As individuals age, they experience increased difficulties producing speech, especially with infrequent words. Older adults report that word retrieval difficulties frequently occur and are highly frustrating. However, little is known about how age affects the neural basis of language production. Moreover, age-related increases in brain activation are often observed, yet there is disagreement about whether such increases represent a form of neural compensation or dedifferentiation. We used functional magnetic resonance imaging (fMRI) to determine if there are age-related differences in functional activation during picture naming and whether such differences are consistent with a compensatory, dedifferentiation, or hybrid account that factors in difficulty. Healthy younger and older adults performed a picture-naming task with stimuli that varied in lexical frequency-our proxy for difficulty. Both younger and older adults were sensitive to lexical frequency behaviorally and neurally. However, younger adults performed more accurately overall and engaged both language (bilateral insula and temporal pole) and cognitive control (bilateral superior frontal gyri and left cingulate) regions to a greater extent than older adults when processing lower frequency items. In both groups, poorer performance was associated with increases in functional activation consistent with dedifferentiation. Moreover, there were age-related differences in the strength of these correlations, with better performing younger adults modulating the bilateral insula and temporal pole and better performing older adults modulating bilateral frontal pole and precuneus. Overall, these findings highlight the influence of task difficulty on fMRI activation in older adults and suggest that as task difficulty increases, older and younger adults rely on different neural resources. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Memory for the usual: the influence of schemas on memory for non-schematic information in younger and older adults.

Schemas are abstract mental representations that influence perceptual and memory processes. Schemas can aide memory for information that is related or congruent with a given schema (i.e., schematic information), yet it is unclear how schemas affect memory for information that does not directly relate to the schema (i.e., non-schematic information). Using a novel scene paradigm, the current series of studies investigated how schemas affect memory for schematic and non-schematic information, as well as how directed encoding influences remembering of both types of information in younger and older adults. Results showed poorer accurate recognition of non-schematic information relative to schematic information, influenced largely by a bias in identifying non-schematic items as "new". While directed encoding was able to increase remembering of non-schematic information and decrease bias across both age groups, the present set of studies highlights the pervasive influence of a schema on memory for non-schematic information.

Shared neural recruitment across working memory and motor control tasks as a function of task difficulty and age.

Past research suggests that working memory (WM) and motor control may engage similar cognitive and neural mechanisms in older adults, particularly when task difficulty increases. However, much of this evidence arises from comparisons across behavioral and imaging studies that test only one of the foregoing functional domains. The current study used fMRI within the same group of older adults to investigate whether WM and motor control recruit common mechanisms, and whether recruitment increased with task demand and age. A conjunction analysis across WM and motor tasks revealed engagement of several frontoparietal regions as a function of increasing task demand. A separate conjunction analysis which included age as a predictor showed comparable regions exhibit increased recruitment with both increasing task demand and age. Results suggest that the recruitment of common frontoparietal regions across WM and motor tasks in response to task difficulty is maintained across the older adult lifespan.

Different types of associative encoding evoke differential processing in both younger and older adults: Evidence from univariate and multivariate analyses.

Age-related deficits in associative processing are well-documented (e.g., Naveh-Benjamin, 2000) and have been assumed to be the result of a general deficit that affects all types of binding. However, recent behavioral research has indicated that the visual configuration of the information that is presented to older adults influences the degree to which this binding deficit is exhibited by older adults (Overman, Dennis et al, 2019; Overman, Dennis, et al., 2018). The purpose of the present study was to further clarify the neural underpinnings of the associative deficit in aging and to examine whether functional activity at encoding differs with respect to the visual configuration and the type of associative being encoded. Using both univariate and multi-voxel pattern analysis, we found differences in both the magnitude of activation and pattern of neural responses associated with the type of association encoded (item-item and item-context). Specifically, our results suggest that, when controlling for stimuli composition, patterns of activation in sensory and frontal regions within the associative encoding network are able to distinguish between different types of associations. With respect to the MTL, multivariate results suggest that only patterns of activation in the PrC in older, but not younger adults, can distinguish between associations types. These findings extend prior work regarding the neural basis of associative memory in young and older adults, and extends the predictions of the binding of item and context model (BIC; Diana, Yonelinas, Ranganath, 2007) to older adults.

Sensory Representations Supporting Memory Specificity: Age Effects on Behavioral and Neural Discriminability.

Older adults' difficulty in distinguishing between old and new information contributes to memory decline, which may occur because older adults are less likely than young adults to retrieve specific sensory details necessary to distinguish between similar items. In male and female human subjects, the present study measured the extent of age differences in the specificity of memory representations using a false memory paradigm in which studied items were linked to retrieval items at multiple levels of similarity. Older adults showed poorer behavioral discrimination than young adults, driven primarily by false recognition of lures that differed from targets only in perceptual details. Patterns of activation across several regions within ventral visual cortex could be used to distinguish between targets and lures when they differed in both perceptual details and a semantic label. However, of ventral visual regions, only signals in the midline occipital cortex could be used to distinguish targets from lures when they differed only in perceptual details. Although there was an overall age deficit for this neural discrimination in this region, the positive relationship between neural and behavioral discriminability did not differ across age groups. In contrast, age moderated the relationship between neural and behavioral discriminability in lateral occipital and fusiform cortices, suggesting that activation patterns within these regions represent different types of information in each age group. Therefore, the quality of perceptual signals is a key contributor to memory discrimination across age groups, with evidence that age differences in the nature of representations emerges outside early visual cortex.SIGNIFICANCE STATEMENT Age-related memory decline is due in part to older adults' difficulties in discriminating between old and new information. We tested whether this deficit arises from lack of specificity in the sensory representations underlying older adults' recognition judgments. Using pattern classification analyses in ventral visual cortices, we found that signals in a region early in the visual stream could distinguish between targets and lures at the highest level of similarity. The discriminability of targets and lures in this region was positively related to behavioral discriminability across age groups despite an overall age deficit in classification accuracy. Together, results showed that older adults' memory deficits are related to reduced discriminability of cognitive processes (old/new recognition) in portions of visual cortex.

Differentiating True and False Schematic Memories in Older Adults.

OBJECTIVE: While schemas aid memory for schematically related information, the gist induced by the schema can also lead to high rates of false memories, especially in older adults. The neural mechanisms that support and differentiate true and false memories in aging are not well understood. The current study sought to clarify this, using a novel scene paradigm to investigate the role of schemas on true and false memories in older adults. METHODS: Healthy older adults encoded schematic scenes (e.g., bathroom). At retrieval, participants were tested on their memory for both schematic and nonschematic targets and lures while functional magnetic resonance imaging data was collected. RESULTS: Results indicate that true memories were supported by the typical retrieval network, and activity in this network was greater for true than false memories. Schema specific retrieval was supported by medial prefrontal cortex, extending this common finding to aging. While no region differentiated false memories compared to correct rejections, results showed that individual differences in false memory rates were associated with variability in neural activity. DISCUSSION: The findings underscore the importance of elucidating the neural basis of cognition within older adults, as well as the specific contribution of individual differences to the neural basis of memory errors in aging.

Same face, same place, different memory: manner of presentation modulates the associative deficit in older adults.

One of the more severe and consequential memory impairments experienced by older adults is the loss of the ability to form and remember associations. Although the associative deficit is often assumed to be unitary, memory episodes may contain different types of associations (e.g., item-item, item-context). Research in younger adults suggests that these different association types may involve different neural mechanisms. This raises the possibility that different association types are not equally affected by aging. In order to investigate this, the current study directly compared memory across item-item and item-context associations in younger and older adults by manipulating the manner of presentation of the associations. Results indicate that the associative deficit in aging is not uniform and that aging has a greater impact on item-context compared to item-item associations. The results have implications for theories of associative memory, age-related cognitive decline, and the functional organization of the medial temporal lobe in aging.

The Effects of Useful Field of View Training on Brain Activity and Connectivity.

OBJECTIVES: Useful Field of View training (UFOVt) is an adaptive computerized cognitive intervention that improves visual attention and transfers to maintained health and everyday functioning in older adults. Although its efficacy is well established, the neural mechanisms underlying this intervention are unknown. This pilot study used functional MRI (fMRI) to explore neural changes following UFOVt. METHOD: Task-driven and resting-state fMRI were used to examine changes in brain activity and connectivity in healthy older adults randomized to 10 hr of UFOVt (n = 13), 10 hr of cognitively stimulating activities (CSA; n = 11), or a no-contact control (NC; n = 10). RESULTS: UFOVt resulted in reduced task-driven activity in the majority of regions of interest (ROIs) associated with task performance, CSA resulted in reduced activity in one ROI, and there were no changes within the NC group. Relative to NC, UFOVt reduced activity in ROIs involved in effortful information processing. There were no other significant between-group task-based differences. Resting-state functional connectivity between ROIs involved in executive function and visual attention was strengthened following UFOVt compared with CSA and NC. DISCUSSION: UFOVt enhances connections needed for visual attention. Together with prior work, this study provides evidence that improvement of the brain's visual attention efficiency is one mechanism underlying UFOVt.