Successful Memory Performance Research Articles

Neural dynamics underlying successful auditory short-term memory performance.

Listeners often operate in complex acoustic environments, consisting of many concurrent sounds. Accurately encoding and maintaining such auditory objects in short-term memory is crucial for communication and scene analysis. Yet, the neural underpinnings of successful auditory short-term memory (ASTM) performance are currently not well understood. To elucidate this issue, we presented a novel, challenging auditory delayed match-to-sample task while recording MEG. Human participants listened to 'scenes' comprising three concurrent tone pip streams. The task was to indicate, after a delay, whether a probe stream was present in the just-heard scene. We present three key findings: First, behavioural performance revealed faster responses in correct versus incorrect trials as well as in 'probe present' versus 'probe absent' trials, consistent with ASTM search. Second, successful compared with unsuccessful ASTM performance was associated with a significant enhancement of event-related fields and oscillatory activity in the theta, alpha and beta frequency ranges. This extends previous findings of an overall increase of persistent activity during short-term memory performance. Third, using distributed source modelling, we found these effects to be confined mostly to sensory areas during encoding, presumably related to ASTM contents per se. Parietal and frontal sources then became relevant during the maintenance stage, indicating that effective STM operation also relies on ongoing inhibitory processes suppressing task-irrelevant information. In summary, our results deliver a detailed account of the neural patterns that differentiate successful from unsuccessful ASTM performance in the context of a complex, multi-object auditory scene.

Estradiol and the Catechol-o-methyltransferase Gene Interact to Predict Working Memory Performance: A Replication and Extension.

Decades of evidence across taxa have established the importance of dopamine (DA) signaling in the pFC for successful working memory performance. Genetic and hormonal factors can shape individual differences in prefrontal DA tone. The catechol-o-methyltransferase (COMT) gene regulates basal prefrontal DA, and the sex hormone 17β-estradiol potentiates DA release. E. Jacobs and M. D'Esposito [Estrogen shapes dopamine-dependent cognitive processes: Implications for women's health. Journal of Neuroscience, 31, 5286-5293, 2011] investigated the moderating role of estradiol on cognition using the COMT gene and COMT enzymatic activity as a proxy for pFC DA tone. They found that increases in 17β-estradiol within women at two time points during the menstrual cycle influenced working memory performance in a COMT-dependent manner. Here, we aimed to replicate and extend the behavioral findings of Jacobs and D'Esposito by employing an intensive repeated-measures design across a full menstrual cycle. Our results replicated the original investigation. Within-person increases in estradiol were associated with improved performance on 2-back lure trials for participants with low basal levels of DA (Val/Val carriers). The association was in the opposite direction for participants with higher basal levels of DA (Met/Met carriers). Our findings support the role of estrogen in DA-related cognitive functions and further highlight the need to consider gonadal hormones in cognitive science research.

Working memory is supported by learning to represent items as actions.

Working memory is typically described as a set of processes that allow for the maintenance and manipulation of information for proximal actions, yet the "action" portion of this construct is commonly overlooked. In contrast, neuroscience-informed theories of working memory have emphasized the hierarchical nature of memory representations, including both goals and sensory representations. These two representational domains are combined for the service of actions. Here, we tested whether, as it is commonly measured (i.e., with computer-based stimuli and button-based responses), working memory involved the planning of motor actions (i.e., specific button presses). Next, we examined the role of motor plan learning in successful working memory performance. Results showed that visual working memory performance was disrupted by unpredictable motor mappings, indicating a role for motor planning in working memory. Further, predictable motor mappings were in fact learned over the course of the experiment, thereby causing the measure of working memory to be partially a measure of participants' ability to learn arbitrary associations between visual stimuli and motor responses. Such learning was not highly specific to certain mappings; in sequences of short tasks, participants improved in their abilities to learn to represent items as actions in working memory. We discuss implications for working memory theories in light of hierarchical structure learning and ecological validity.

How Consumers Process Unexpected Online Advertisements

The distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Thirty-five younger (18-27 years old) and 32 older (67-75 years old) women and men incidentally encoded images of faces and houses, followed by an old/new recognition memory task. During encoding, age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built on high item stability, that is, high representational similarity between initial and repeated presentation of an item, which was greater in younger than older adults. Overall, we found that differences in representational distinctiveness coexist across representational levels and contribute to interindividual and intraindividual variability in memory success, with item specificity being the strongest contributor. Our results close an important gap in the literature, showing that older adults9 neural representation of item-specific information in addition to categorical information is reduced compared with younger adults. <b>SIGNIFICANCE STATEMENT</b> A long-standing hypothesis links age-related cognitive decline to a loss of neural specificity. While previous evidence supports the notion of age-related neural dedifferentiation of category-level information in ventral visual cortex, whether or not age differences exist at the item level was a matter of debate. Here, we observed age group differences at both levels as well as associations between both categorical distinctiveness and item specificity to memory performance, with item specificity being the strongest contributor. Importantly, age differences in occipital item specificity were largely due to reduced item stability across repetitions in older adults. Our results suggest that age differences in neural representations can be observed across the entire cortical hierarchy and are not limited to category-level information.

Children show adult-like hippocampal pattern similarity for familiar but not novel events

The ability to detect differences among similar events in our lives is a crucial aspect of successful episodic memory performance, which develops across early childhood. The neural substrate of this ability is supported by operations in the medial temporal lobe (MTL). Here, we used representational similarity analysis (RSA) to measure neural pattern similarity in hippocampus, perirhinal cortex, and parahippocampal cortex for 4- to 10-year-old children and adults during naturalistic viewing of clips from the same compared to different movies. Further, we assessed the role of prior exposure to individual movie clips on pattern similarity in the MTL. In both age groups, neural pattern similarity in hippocampus was lower for clips drawn from the same movies compared to those drawn from different movies, suggesting that related content activates processes focused on keeping representations with shared content distinct. However, children showed this only for movies with which they had prior exposures, whereas adults showed the effect regardless of any prior exposures to the movies. These findings suggest that children require repeated exposure to stimuli to show adult-like MTL functioning in distinguishing among similar events.

Greater sleep variance related to decrements in memory performance and event-specific neural similarity: a racially/ethnically diverse lifespan sample

Successful memory performance depends on overlap between neural representations at encoding and retrieval. With older age, neural similarity, memory performance, and sleep quality decline. Regardless of age, racial/ethnic minorities tend to experience poor sleep, which may contribute to poor memory. Previous studies have not investigated memory performance, neural similarity, sleep quality, and age in diverse participants. Here, we recruited racially/ethnically diverse adults across the lifespan and examined night-to-night sleep quality in relation to memory performance and encoding-retrieval similarity. We employed item-specific, representational similarity analysis (not confounded by effort, word perception, or differences in electroencephalography signal amplitude) to assess neural similarity for intact and recombined paired associates. Greater sleep variance and poorer memory performance were more strongly associated with older age. Interestingly, sleep variance was positively associated with neural similarity for intact pairs. This relationship was stronger with younger age and for racial/ethnic minorities. For recombined pairs, greater sleep variance was associated with reduced neural similarity. Thus, varied sleep may induce greater reliance on familiarity, while consistent sleep may support recollection.

P396. Altered Prefrontal-Thalamo-Hippocampal Synchrony During a Working Memory Task in SETD1A-Deficient Mice

Heterozygous null mutations of SETD1A are definitively linked to increased schizophrenia risk in humans. Mice carrying similar mutations reportedly show deficits in spatial working memory, a cognitive function disrupted in schizophrenia. To explore the neurobiological consequences of SETD1A haploinsufficiency, we examined synchrony across neural circuits containing the medial prefrontal cortex (mPFC), nucleus reuniens (Re) of the thalamus, and ventral and dorsal hippocampus (vHPC, dHPC), four regions necessary for successful working memory performance in rodents.

The olfactory bulb modulates entorhinal cortex oscillations during spatial working memory

Cognitive functions such as working memory require integrated activity among different brain regions. Notably, entorhinal cortex (EC) activity is associated with the successful working memory task. Olfactory bulb (OB) oscillations are known as rhythms that modulate rhythmic activity in widespread brain regions during cognitive tasks. Since the OB is structurally connected to the EC, we hypothesized that OB could modulate EC activity during working memory performance. Herein, we explored OB–EC functional connectivity during spatial working memory performance by simultaneous recording local field potentials when rats performed a Y-maze task. Our results showed that the coherence of delta, theta, and gamma-band oscillations between OB and EC was increased during correct trials compared to wrong trials. Cross-frequency coupling analyses revealed that the modulatory effect of OBs low-frequency phase on EC gamma power and phase was enhanced when animals correctly performed working memory task. The influx of information from OB to EC was also increased at delta and gamma bands within correct trials. These findings indicated that the modulatory influence of OB rhythms on EC oscillations might be necessary for successful working memory performance.

Anterior Thalamic Inputs Are Required for Subiculum Spatial Coding, with Associated Consequences for Hippocampal Spatial Memory.

Just as hippocampal lesions are principally responsible for “temporal lobe” amnesia, lesions affecting the anterior thalamic nuclei seem principally responsible for a similar loss of memory, “diencephalic” amnesia. Compared with the former, the causes of diencephalic amnesia have remained elusive. A potential clue comes from how the two sites are interconnected, as within the hippocampal formation, only the subiculum has direct, reciprocal connections with the anterior thalamic nuclei. We found that both permanent and reversible anterior thalamic nuclei lesions in male rats cause a cessation of subicular spatial signaling, reduce spatial memory performance to chance, but leave hippocampal CA1 place cells largely unaffected. We suggest that a core element of diencephalic amnesia stems from the information loss in hippocampal output regions following anterior thalamic pathology.SIGNIFICANCE STATEMENT At present, we know little about interactions between temporal lobe and diencephalic memory systems. Here, we focused on the subiculum, as the sole hippocampal formation region directly interconnected with the anterior thalamic nuclei. We combined reversible and permanent lesions of the anterior thalamic nuclei, electrophysiological recordings of the subiculum, and behavioral analyses. Our results were striking and clear: following permanent thalamic lesions, the diverse spatial signals normally found in the subiculum (including place cells, grid cells, and head-direction cells) all disappeared. Anterior thalamic lesions had no discernible impact on hippocampal CA1 place fields. Thus, spatial firing activity within the subiculum requires anterior thalamic function, as does successful spatial memory performance. Our findings provide a key missing part of the much bigger puzzle concerning why anterior thalamic damage is so catastrophic for spatial memory in rodents and episodic memory in humans.

Impaired posterior cingulate cortex-parahippocampus connectivity is associated with episodic memory retrieval problems in amnestic mild cognitive impairment.

Episodic memory retention and retrieval decline are the most common impairments observed in amnestic mild cognitive impairment (aMCI) patients who progress to Alzheimer's disease (AD). Clinical electroencephalography research shows that patients with dementia due to AD exhibit a slowing of neural electrical activity in the parietal cortex. Memory research has further suggested that successful memory performance is associated with changes in a posterior cingulate-parahippocampal cortical network together with increased θ-γ oscillatory coupling, where θ oscillations act as carrier waves for γ oscillations, which contain the actual information. However, the neurophysiological link between the memory research and clinical studies investigating aMCI and AD is lacking. In this study, we look at brain activity in aMCI and how it relates to memory performance. We demonstrate decreased γ power in the posterior cingulate cortex and the left and right parahippocampus in aMCI patients in comparison to control participants. This goes together with reduced θ coherence between the posterior cingulate cortex and parahippocampus associated with altered memory performance aMCI patients in comparison to control participants. In addition, comparing patients with aMCI to control participants reveals an effect for θ-γ coupling for the posterior cingulate cortex, and the left and right parahippocampus. Taken together, our results show that parahippocampus and posterior cingulate cortex interact via θ-γ coupling, which is associated with memory recollection and is altered in aMCI patients, offering a potential candidate mechanism for memory decline in aMCI.

Temporal Regularity May Not Improve Memory for Item-Specific Detail.

Regularities in event timing allow for the allocation of attention to critical time-points when an event is most likely to occur, leading to improved visual perception. Results from recent studies indicate that similar benefits may extend to memory for scenes and objects. Here, we investigated whether benefits of temporal regularity are evident when detailed, item-specific representations are necessary for successful recognition memory performance. In Experiments 1 and 2, pictures of objects were presented with either predictable or randomized event timing, in separate encoding blocks. In the test phase, old and new objects were presented, intermixed with perceptually similar exemplars of encoded objects. In Experiment 3 we attempted to replicate previously reported memory enhancements for scenes. In contrast to predictions, temporal regularity did not affect response times (RT) or improve recognition memory accuracy in any of our experiments. These results suggest that any effects of temporal expectation on memory are subtle and may be sensitive to minor changes in task parameters. In sum, indirect upregulation of attention through imposed temporal structure may not be sufficient to have downstream effects on memory performance.

Tracking Age Differences in Neural Distinctiveness across Representational Levels.

The distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Thirty-five younger (18-27 years old) and 32 older (67-75 years old) women and men incidentally encoded images of faces and houses, followed by an old/new recognition memory task. During encoding, age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built on high item stability, that is, high representational similarity between initial and repeated presentation of an item, which was greater in younger than older adults. Overall, we found that differences in representational distinctiveness coexist across representational levels and contribute to interindividual and intraindividual variability in memory success, with item specificity being the strongest contributor. Our results close an important gap in the literature, showing that older adults' neural representation of item-specific information in addition to categorical information is reduced compared with younger adults.SIGNIFICANCE STATEMENT A long-standing hypothesis links age-related cognitive decline to a loss of neural specificity. While previous evidence supports the notion of age-related neural dedifferentiation of category-level information in ventral visual cortex, whether or not age differences exist at the item level was a matter of debate. Here, we observed age group differences at both levels as well as associations between both categorical distinctiveness and item specificity to memory performance, with item specificity being the strongest contributor. Importantly, age differences in occipital item specificity were largely due to reduced item stability across repetitions in older adults. Our results suggest that age differences in neural representations can be observed across the entire cortical hierarchy and are not limited to category-level information.

Theta and alpha oscillatory responses differentiate between six-to seven-year-old children and adults during successful visual and auditory memory encoding

The healthy maturation of the brain is one of the intriguing topics that need to be investigated to understand human brain and child development. The present study aimed to investigate the development of memory processes both for auditory and visual memory using electroencephalography (EEG)-Brain Dynamics methodologies.Sixteen healthy children between the ages of 6 and 7 years and eighteen healthy young adults (age: 21.32 ± 3.28 years) were included in the study. EEG was recorded from 18 channels during the visual and auditory memory paradigms. Two different subtests of the WISC-IV IQ test were applied to all children. Event-related theta (4–7 Hz), alpha (8–13 Hz) power and phase-locking were analyzed.The young adults had higher memory performance than the children for both auditory and visual paradigms. The children had increased theta phase-locking and left alpha power in response to the remembered objects in comparison to the forgotten objects. The young adults had higher theta and alpha phase-locking than the children over the frontal and central locations (p < 0.05), and the children had higher parietal-occipital alpha phase-locking than the young adults. There was an increase in alpha power in children, whereas young adults had decreased post-stimulus alpha power in response to memory paradigms.The present study showed that frontocentral theta and alpha phase-locking had an essential role in brain maturation and successful memory performance. Event-related theta and alpha responses could be one of the important indicators of the mature and healthy brain, and these responses could change depending on the maturation state and age.

Phase-dependent amplification of working memory content and performance

Successful working memory performance has been related to oscillatory mechanisms operating in low-frequency ranges. Yet, their mechanistic interaction with the distributed neural activity patterns representing the content of the memorized information remains unclear. Here, we record EEG during a working memory retention interval, while a task-irrelevant, high-intensity visual impulse stimulus is presented to boost the read-out of distributed neural activity related to the content held in working memory. Decoding of this activity with a linear classifier reveals significant modulations of classification accuracy by oscillatory phase in the theta/alpha ranges at the moment of impulse presentation. Additionally, behavioral accuracy is highest at the phases showing maximized decoding accuracy. At those phases, behavioral accuracy is higher in trials with the impulse compared to no-impulse trials. This constitutes the first evidence in humans that working memory information is maximized within limited phase ranges, and that phase-selective, sensory impulse stimulation can improve working memory.

The Neural Mechanisms of Associative Memory Revisited: fMRI Evidence from Implicit Contingency Learning

The literature describes a basic neurofunctional antagonism between episodic memory encoding and retrieval with opposed patterns of neural activation and deactivation, particularly in posterior midline regions. This has been coined the encoding/retrieval (E/R) flip. The present fMRI study uses an innovative task paradigm to further elucidate neurofunctional relations of encoding and retrieval in associative memory. Thereby, memory encoding is implemented as implicit (non-deliberate) cognitive process, whereas the prior literature focused mainly on explicit encoding. Moreover, instead of defining brain activations related to successful (vs. unsuccessful) memory performance, the task paradigm provides proper no-memory baseline conditions. More specifically, the encoding task includes trials with non-contingent (not learnable) stimulus combinations, while the retrieval task uses trials with a simple matching exercise with no mnemonic requirements. The analyses revealed circumscribed activation in the posterior middle cingulate cortex (pMCC) together with prominent deactivation in the anterior insula cortex (aIC) as core neural substrate of implicit memory encoding. Thereby, the pMCC exhibited positive functional connectivity to the hippocampus. Memory retrieval was related to an activation pattern exactly opposed to memory encoding with deactivation in the pMCC and activation in the aIC, while the aIC additionally exhibited a negative (i.e., arguably inhibitive) functional connectivity to the pMCC. Important to note, the observed pattern of activations/de-activations in the pMCC appears to conflict with prevalent E/R flip findings. The outlined results and their (alleged) discrepancies with prior study reports are discussed primarily in the context of the default mode network’s functioning and its context-sensitive regulation. Finally, we point out the relevance of the present work for the understanding and further investigation of the neurofunctional aberrations occurring during normal and pathological aging.

Balance between Transmitter Availability and Dopamine D2 Receptors in Prefrontal Cortex Influences Memory Functioning.

Insufficient or excessive dopaminergic tone impairs cognitive performance. We examine whether the balance between transmitter availability and dopamine (DA) D2 receptors (D2DRs) is important for successful memory performance in a large sample of adults (n = 175, 64-68years). The Catechol-O-Methyltransferase polymorphism served as genetic proxy for endogenous prefrontal DA availability, and D2DRs in dorsolateral prefrontal cortex (dlPFC) were measured with [11C]raclopride-PET. Individuals for whom D2DR status matched DA availability showed higher levels of episodic and working-memory performance than individuals with insufficient or excessive DA availability relative to the number of receptors. A similar pattern restricted to episodic memory was observed for D2DRs in caudate. Functional magnetic resonance imaging data acquired during working-memory performance confirmed the importance of a balanced DA system for load-dependent brain activity in dlPFC. Our data suggest that the inverted-U-shaped function relating DA signaling to cognition is modulated by a dynamic association between DA availability and receptor status.

Structural and Functional MRI Evidence for Distinct Medial Temporal and Prefrontal Roles in Context-dependent Relational Memory.

Declarative memory is supported by distributed brain networks in which the medial-temporal lobes (MTLs) and pFC serve as important hubs. Identifying the unique and shared contributions of these regions to successful memory performance is an active area of research, and a growing literature suggests that these structures often work together to support declarative memory. Here, we present data from a context-dependent relational memory task in which participants learned that individuals belonged in a single room in each of two buildings. Room assignment was consistent with an underlying contextual rule structure in which male and female participants were assigned to opposite sides of a building and the side assignment switched between buildings. In two experiments, neural correlates of performance on this task were evaluated using multiple neuroimaging tools: diffusion tensor imaging (Experiment 1), magnetic resonance elastography (Experiment 1), and functional MRI (Experiment 2). Structural and functional data from each individual modality provided complementary and consistent evidence that the hippocampus and the adjacent white matter tract (i.e., fornix) supported relational memory, whereas the ventromedial pFC/OFC (vmPFC/OFC) and the white matter tract connecting vmPFC/OFC to MTL (i.e., uncinate fasciculus) supported memory-guided rule use. Together, these data suggest that MTL and pFC structures differentially contribute to and support contextually guided relational memory.

Uncovering a Role for the Dorsal Hippocampal Commissure in Recognition Memory

The dorsal hippocampal commissure (DHC) is a white matter tract that provides interhemispheric connections between temporal lobe brain regions. Despite the importance of these regions for learning and memory, there is scant evidence of a role for the DHC in successful memory performance. We used diffusion-weighted magnetic resonance imaging (DW-MRI) and white matter tractography to reconstruct the DHC in both humans (in vivo) and nonhuman primates (ex vivo). Across species, our findings demonstrate a close consistency between the known anatomy and tract reconstructions of the DHC. Anterograde tract-tracer techniques also highlighted the parahippocampal origins of DHC fibers in nonhuman primates. Finally, we derived diffusion tensor MRI metrics from the DHC in a large sample of human subjects to investigate whether interindividual variation in DHC microstructure is predictive of memory performance. The mean diffusivity of the DHC correlated with performance in a standardized recognition memory task, an effect that was not reproduced in a comparison commissure tract—the anterior commissure. These findings highlight a potential role for the DHC in recognition memory, and our tract reconstruction approach has the potential to generate further novel insights into the role of this previously understudied white matter tract in both health and disease.

Intraindividual Variability in Inhibition and Prospective Memory in Healthy Older Adults: Insights from Response Regularity and Rapidity

Successful prospective memory (PM) performance relies on executive functions, including inhibition. However, PM and inhibition are usually assessed in separate tasks, and analytically the focus is either on group differences or at most on interindividual differences. Conjoint measures of PM and inhibition performance that take into account intraindividual variability (IIV) are thus missing. In the present study, we assessed healthy older adults’ level of performance and IIV in both inhibition and PM using a classical Go/NoGo task. We also created a prospective Go/NoGo version that embeds a PM component into the task. Using dynamic structural equation modeling, we assessed the joint effects of mean level (), an indicator of amplitude of fluctuations in IIV (or net IIV; intraindividual standard deviation, iSD), and an indicator of time dependency in IIV (the autoregressive parameter ) in reaction times (RTs) on inhibition and PM performance. Results indicate that higher inhibition failure, but not IIV, predicted PM errors, corroborating the current literature on the involvement of prepotent response inhibition in PM processes. In turn, fastest RT latency () and increased net IIV (iSD) were consistently associated with prepotent response inhibition failure, while coherence in RT pattern () was beneficial to inhibition performance when the task was novel. Time-dependent IIV () appears to reflect an adaptive exploration of strategies to attain optimal performance, whereas increased net IIV (iSD) may indicate inefficient sustained cognitive processes when performance is high. We discuss trade-off processes between competing tasks.

An Event Related Potentials Study of Semantic Coherence Effect during Episodic Encoding in Schizophrenia Patients.

The objective of this electrophysiological study was to investigate the processing of semantic coherence during encoding in relation to episodic memory processes promoted at test, in schizophrenia patients, by using the N400 paradigm. Eighteen schizophrenia patients and 15 healthy participants undertook a recognition memory task. The stimuli consisted of pairs of words either semantically related or unrelated to a given category name (context). During encoding, both groups exhibited an N400 external semantic coherence effect. Healthy controls also showed an N400 internal semantic coherence effect, but this effect was not present in patients. At test, related stimuli were accompanied by an FN400 old/new effect in both groups and by a parietal old/new effect in the control group alone. In the patient group, external semantic coherence effect was associated with FN400, while, in the control group, it was correlated to the parietal old/new effect. Our results indicate that schizophrenia patients can process the contextual information at encoding to enhance familiarity process for related stimuli at test. Therefore, cognitive rehabilitation therapies targeting the implementation of semantic encoding strategies can mobilize familiarity which in turn can overcome the recollection deficit, promoting successful episodic memory performance in schizophrenia patients.