The Encoding/Retrieval Flip: Interactions between Memory Performance and Memory Stage and Relationship to Intrinsic Cortical Networks

fMRI studies have linked the posteromedial cortex to episodic learning (encoding) and remembering (retrieval) processes. The posteromedial cortex is considered part of the default network and tends to deactivate during encoding but activate during retrieval, a pattern known as the encoding/retrieval flip. Yet, the exact relationship between the neural correlates of memory performance (hit/miss) and memory stage (encoding/retrieval) and the extent of overlap with intrinsic cortical networks remains to be elucidated. Using task-based fMRI, we isolated the pattern of activity associated with memory performance, memory stage, and the interaction between both. Using resting-state fMRI, we identified which intrinsic large-scale functional networks overlapped with regions showing task-induced effects. Our results demonstrated an effect of successful memory performance in regions associated with the control network and an effect of unsuccessful memory performance in the ventral attention network. We found an effect of memory retrieval in brain regions that span the default and control networks. Finally, we found an interaction between memory performance and memory stage in brain regions associated with the default network, including the posteromedial cortex, posterior parietal cortex, and parahippocampal cortex. We discuss these findings in relation to the encoding/retrieval flip. In general, the findings demonstrate that task-induced effects cut across intrinsic cortical networks. Furthermore, regions within the default network display functional dissociations, and this may have implications for the neural underpinnings of age-related memory disorders.

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Selective Development of Anticorrelated Networks in the Intrinsic Functional Organization of the Human Brain

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00517 ◽

2014 ◽

Vol 26 (3) ◽

pp. 501-513 ◽

Cited By ~ 99

Author(s):

Xiaoqian J. Chai ◽

Noa Ofen ◽

John D. E. Gabrieli ◽

Susan Whitfield-Gabrieli

Keyword(s):

Functional Organization ◽

Resting State Fmri ◽

Brain Regions ◽

Motion Artifacts ◽

Default Network ◽

Age Related ◽

Large Growth ◽

Multiple Regions ◽

Medial Pfc ◽

Positive Correlations

We examined the normal development of intrinsic functional connectivity of the default network (brain regions typically deactivated for attention-demanding tasks) as measured by resting-state fMRI in children, adolescents, and young adults ages 8–24 years. We investigated both positive and negative correlations and employed analysis methods that allowed for valid interpretation of negative correlations and that also minimized the influence of motion artifacts that are often confounds in developmental neuroimaging. As age increased, there were robust developmental increases in negative correlations, including those between medial pFC (MPFC) and dorsolateral pFC (DLPFC) and between lateral parietal cortices and brain regions associated with the dorsal attention network. Between multiple regions, these correlations reversed from being positive in children to negative in adults. Age-related changes in positive correlations within the default network were below statistical threshold after controlling for motion. Given evidence in adults that greater negative correlation between MPFC and DLPFC is associated with superior cognitive performance, the development of an intrinsic anticorrelation between MPFC and DLPFC may be a marker of the large growth of working memory and executive functions that occurs from childhood to young adulthood.

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Inefficient Encoding as an Explanation for Age-Related Deficits in Recollection-Based Processing

Journal of Psychophysiology ◽

10.1027/0269-8803/a000122 ◽

2014 ◽

Vol 28 (3) ◽

pp. 148-161 ◽

Cited By ~ 12

Author(s):

David Friedman ◽

Ray Johnson

Keyword(s):

Older Adults ◽

Young Adults ◽

Cognitive Processes ◽

Brain Activity ◽

Memory Performance ◽

Brain Regions ◽

Semantic Retrieval ◽

Age Related ◽

The Face ◽

Episodic Memories

A cardinal feature of aging is a decline in episodic memory (EM). Nevertheless, there is evidence that some older adults may be able to “compensate” for failures in recollection-based processing by recruiting brain regions and cognitive processes not normally recruited by the young. We review the evidence suggesting that age-related declines in EM performance and recollection-related brain activity (left-parietal EM effect; LPEM) are due to altered processing at encoding. We describe results from our laboratory on differences in encoding- and retrieval-related activity between young and older adults. We then show that, relative to the young, in older adults brain activity at encoding is reduced over a brain region believed to be crucial for successful semantic elaboration in a 400–1,400-ms interval (left inferior prefrontal cortex, LIPFC; Johnson, Nessler, & Friedman, 2013 ; Nessler, Friedman, Johnson, & Bersick, 2007 ; Nessler, Johnson, Bersick, & Friedman, 2006 ). This reduced brain activity is associated with diminished subsequent recognition-memory performance and the LPEM at retrieval. We provide evidence for this premise by demonstrating that disrupting encoding-related processes during this 400–1,400-ms interval in young adults affords causal support for the hypothesis that the reduction over LIPFC during encoding produces the hallmarks of an age-related EM deficit: normal semantic retrieval at encoding, reduced subsequent episodic recognition accuracy, free recall, and the LPEM. Finally, we show that the reduced LPEM in young adults is associated with “additional” brain activity over similar brain areas as those activated when older adults show deficient retrieval. Hence, rather than supporting the compensation hypothesis, these data are more consistent with the scaffolding hypothesis, in which the recruitment of additional cognitive processes is an adaptive response across the life span in the face of momentary increases in task demand due to poorly-encoded episodic memories.

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Resting‐State EEG Microstates Parallel Age‐Related Differences in Allocentric Spatial Working Memory Performance

Brain Topography ◽

10.1007/s10548-021-00835-3 ◽

2021 ◽

Author(s):

Adeline Jabès ◽

Giuliana Klencklen ◽

Paolo Ruggeri ◽

Christoph M. Michel ◽

Pamela Banta Lavenex ◽

...

Keyword(s):

Older Adults ◽

Working Memory ◽

Resting State ◽

Cognitive Aging ◽

Temporal Dynamics ◽

Spatial Working Memory ◽

Brain Activity ◽

Memory Performance ◽

Brain Regions ◽

Age Related

AbstractAlterations of resting-state EEG microstates have been associated with various neurological disorders and behavioral states. Interestingly, age-related differences in EEG microstate organization have also been reported, and it has been suggested that resting-state EEG activity may predict cognitive capacities in healthy individuals across the lifespan. In this exploratory study, we performed a microstate analysis of resting-state brain activity and tested allocentric spatial working memory performance in healthy adult individuals: twenty 25–30-year-olds and twenty-five 64–75-year-olds. We found a lower spatial working memory performance in older adults, as well as age-related differences in the five EEG microstate maps A, B, C, C′ and D, but especially in microstate maps C and C′. These two maps have been linked to neuronal activity in the frontal and parietal brain regions which are associated with working memory and attention, cognitive functions that have been shown to be sensitive to aging. Older adults exhibited lower global explained variance and occurrence of maps C and C′. Moreover, although there was a higher probability to transition from any map towards maps C, C′ and D in young and older adults, this probability was lower in older adults. Finally, although age-related differences in resting-state EEG microstates paralleled differences in allocentric spatial working memory performance, we found no evidence that any individual or combination of resting-state EEG microstate parameter(s) could reliably predict individual spatial working memory performance. Whether the temporal dynamics of EEG microstates may be used to assess healthy cognitive aging from resting-state brain activity requires further investigation.

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Neurocognitive Aging and Functional Connectivity Using Functional Magnetic Resonance Imaging

Oxford Research Encyclopedia of Psychology ◽

10.1093/acrefore/9780190236557.013.385 ◽

2018 ◽

Author(s):

Hana Burianová

Keyword(s):

Functional Connectivity ◽

Cognitive Processes ◽

Large Scale ◽

Healthy Aging ◽

Brain Activity ◽

Brain Regions ◽

Effective Strategies ◽

Cognitive Improvement ◽

Age Related ◽

Neurocognitive Aging

Determining the mechanisms that underlie neurocognitive aging, such as compensation or dedifferentiation, and facilitating the development of effective strategies for cognitive improvement is essential due to the steadily rising aging population. One approach to study the characteristics of healthy aging comprises the assessment of functional connectivity, delineating markers of age-related neurocognitive plasticity. Functional connectivity paradigms characterize complex one-to-many (or many-to-many) structure–function relations, as higher-level cognitive processes are mediated by the interaction among a number of functionally related neural areas rather than localized to discrete brain regions. Task-related or resting-state interregional correlations of brain activity have been used as reliable indices of functional connectivity, delineating age-related alterations in a number of large-scale brain networks, which subserve attention, working memory, episodic retrieval, and task-switching. Together with behavioral and regional activation studies, connectivity studies and modeling approaches have contributed to our understanding of the mechanisms of age-related reorganization of distributed functional networks; specifically, reduced neural specificity (dedifferentiation) and associated impairment in inhibitory control and compensatory neural recruitment.

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Organization of Propagated Intrinsic Brain Activity in Individual Humans

Cerebral Cortex ◽

10.1093/cercor/bhz198 ◽

2019 ◽

Vol 30 (3) ◽

pp. 1716-1734 ◽

Cited By ~ 10

Author(s):

Ryan V Raut ◽

Anish Mitra ◽

Scott Marek ◽

Mario Ortega ◽

Abraham Z Snyder ◽

...

Keyword(s):

Resting State ◽

Large Scale ◽

Cortical Excitability ◽

Brain Activity ◽

Resting State Fmri ◽

Brain Regions ◽

Brain Organization ◽

Individual Level ◽

Slow Activity ◽

Lag Structure

Abstract Spontaneous infra-slow (<0.1 Hz) fluctuations in functional magnetic resonance imaging (fMRI) signals are temporally correlated within large-scale functional brain networks, motivating their use for mapping systems-level brain organization. However, recent electrophysiological and hemodynamic evidence suggest state-dependent propagation of infra-slow fluctuations, implying a functional role for ongoing infra-slow activity. Crucially, the study of infra-slow temporal lag structure has thus far been limited to large groups, as analyzing propagation delays requires extensive data averaging to overcome sampling variability. Here, we use resting-state fMRI data from 11 extensively-sampled individuals to characterize lag structure at the individual level. In addition to stable individual-specific features, we find spatiotemporal topographies in each subject similar to the group average. Notably, we find a set of early regions that are common to all individuals, are preferentially positioned proximal to multiple functional networks, and overlap with brain regions known to respond to diverse behavioral tasks—altogether consistent with a hypothesized ability to broadly influence cortical excitability. Our findings suggest that, like correlation structure, temporal lag structure is a fundamental organizational property of resting-state infra-slow activity.

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Functional Connectivity of Hippocampal CA3 Predicts Neurocognitive Aging via CA1–Frontal Circuit

Cerebral Cortex ◽

10.1093/cercor/bhaa008 ◽

2020 ◽

Vol 30 (8) ◽

pp. 4297-4305 ◽

Cited By ~ 3

Author(s):

Xia Liang ◽

Li-Ming Hsu ◽

Hanbing Lu ◽

Jessica A Ash ◽

Peter R Rapp ◽

...

Keyword(s):

Prefrontal Cortex ◽

Functional Connectivity ◽

Memory Performance ◽

Network Connectivity ◽

Resting State Fmri ◽

Cognitive Outcome ◽

Spatial Learning And Memory ◽

Aged Rats ◽

Age Related ◽

Effects Of Aging

Abstract The CA3 and CA1 principal cell fields of the hippocampus are vulnerable to aging, and age-related dysfunction in CA3 may be an early seed event closely linked to individual differences in memory decline. However, whether the differential vulnerability of CA3 and CA1 is associated with broader disruption in network-level functional interactions in relation to age-related memory impairment, and more specifically, whether CA3 dysconnectivity contributes to the effects of aging via CA1 network connectivity, has been difficult to test. Here, using resting-state fMRI in a group of aged rats uncontaminated by neurodegenerative disease, aged rats displayed widespread reductions in functional connectivity of CA3 and CA1 fields. Age-related memory deficits were predicted by connectivity between left CA3 and hippocampal circuitry along with connectivity between left CA1 and infralimbic prefrontal cortex. Notably, the effects of CA3 connectivity on memory performance were mediated by CA1 connectivity with prefrontal cortex. We additionally found that spatial learning and memory were associated with functional connectivity changes lateralized to the left CA3 and CA1 divisions. These results provide novel evidence that network-level dysfunction involving interactions of CA3 with CA1 is an early marker of poor cognitive outcome in aging.

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The more you know: Investigating why adults get a bigger memory boost from semantic congruency than children

10.1101/456624 ◽

2018 ◽

Author(s):

Wei-Chun Wang ◽

Simona Ghetti ◽

Garvin Brod ◽

Silvia A. Bunge

Keyword(s):

Functional Connectivity ◽

Prior Knowledge ◽

Source Memory ◽

Multivariate Analyses ◽

Memory Performance ◽

Memory Task ◽

Neural Substrates ◽

Brain Regions ◽

Age Related ◽

With Memory

AbstractHumans possess the capacity to employ prior knowledge in the service of our ability to remember; thus, memory is oftentimes superior for information that is semantically congruent with our prior knowledge. This congruency benefit grows during development, but little is understood about neurodevelopmental differences that underlie this growth. Here, we sought to explore the brain mechanisms underlying these phenomena. To this end, we examined the neural substrates of semantically congruent vs. incongruent item-context associations in 116 children and 25 young adults who performed encoding and retrieval tasks during functional MRI data collection. Participants encoded item-context pairs by judging whether an item belonged in a scene. Episodic memory was then tested with a source memory task. Consistent with prior work, source memory accuracy improved with age, and was greater for congruent than incongruent pairs; further, this congruency benefit was greater in adults than children. Age-related differences were observed across univariate, functional connectivity, and multivariate analyses, particularly in lateral prefrontal cortex (PFC). In sum, our results revealed two general age differences. First, left ventrolateral/rostrolateral PFC exhibited age-related increases in univariate activity, as well as greater functional connectivity with temporal regions during the processing of congruency. Second, right rostrolateral PFC activation was associated with successfully encoded congruent associations in adults, but not children. Finally, multivariate analyses provided evidence for stronger veridical memory in adults than children in right ventrolateral PFC. These effects in right lateral PFC were significantly correlated with memory performance, implicating them in the process of remembering congruent associations. These results connect brain regions associated with top-down control in the congruency benefit and age-related improvements therein.

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Aging I

Remembering ◽

10.1093/oso/9780192895226.003.0007 ◽

2021 ◽

pp. 169-188

Author(s):

Fergus I. M. Craik

Keyword(s):

Working Memory ◽

Cognitive Control ◽

Healthy Aging ◽

Recall Performance ◽

Memory Performance ◽

Environmental Support ◽

Age Related ◽

Retrieval Processes ◽

Processing Resources ◽

Frontal Lobe Functions

Memory performance declines in the course of healthy aging, and this chapter discusses some reasons why this may be so. The author suggests that there is an age-related decline in both processing resources and in cognitive control, and that these deficiencies underlie less efficient encoding and retrieval processes. Age-related memory losses are greater in some tasks than in others, however, and the case is made that losses are relatively slight in situations that involve substantial amounts of environmental support and therefore require small amounts of self-initiated activity. In turn, the inefficiency of self-initiated activities is attributed to age-related deficiencies in frontal lobe functions. Age-related deficits in recall performance (which is heavily reliant on self-initiation) are reduced in a recognition test, which embodies greater environmental support. Deficits were also reduced by the use of pictures as materials, and there were no age differences in the ability to hold high-valued words in working memory. These effects are illustrated by experiments carried out by the author and collaborators.

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Spatiotemporal functional interactivity among large-scale brain networks

10.1101/2020.04.14.041830 ◽

2020 ◽

Author(s):

Nan Xu ◽

Peter C. Doerschuk ◽

Shella D. Keilholz ◽

R. Nathan Spreng

Keyword(s):

Human Brain ◽

Short Duration ◽

Resting State ◽

Large Scale ◽

Brain Networks ◽

Resting State Fmri ◽

Brain Regions ◽

Spatial Direction ◽

Macro Scale ◽

High Degree

AbstractThe macro-scale intrinsic functional network architecture of the human brain has been well characterized. Early studies revealed robust and enduring patterns of static connectivity, while more recent work has begun to explore the temporal dynamics of these large-scale brain networks. Little work to date has investigated directed connectivity within and between these networks, or the temporal patterns of afferent (input) and efferent (output) connections between network nodes. Leveraging a novel analytic approach, prediction correlation, we investigated the causal interactions within and between large-scale networks of the brain using resting-state fMRI. This technique allows us to characterize information transfer between brain regions in both the spatial (direction) and temporal (duration) scales. Using data from the Human Connectome Project (N=200) we applied prediction correlation techniques to four resting state fMRI runs (total TRs = 4800). Three central observations emerged. First, the strongest and longest duration connections were observed within the somatomotor, visual and dorsal attention networks. Second, the short duration connections were observed for high-degree nodes in the visual and default networks, as well as in hippocampus. Specifically, the connectivity profile of the highest-degree nodes was dominated by efferent connections to multiple cortical areas. Moderate high-degree nodes, particularly in hippocampal regions, showed an afferent connectivity profile. Finally, multimodal association nodes in lateral prefrontal brain regions demonstrated a short duration, bidirectional connectivity profile, consistent with this region’s role in integrative and modulatory processing. These results provide novel insights into the spatiotemporal dynamics of human brain function.

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Human hippocampal CA3 damage disrupts both recent and remote episodic memories

eLife ◽

10.7554/elife.41836 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 7

Author(s):

Thomas D Miller ◽

Trevor T-J Chong ◽

Anne M Aimola Davies ◽

Michael R Johnson ◽

Sarosh R Irani ◽

...

Keyword(s):

Episodic Memory ◽

Medial Temporal Lobe ◽

Memory Performance ◽

Functional Integration ◽

Resting State Fmri ◽

Model Organisms ◽

Default Network ◽

Episodic Retrieval ◽

Graph Theoretic ◽

Episodic Memories

Neocortical-hippocampal interactions support new episodic (event) memories, but there is conflicting evidence about the dependence of remote episodic memories on the hippocampus. In line with systems consolidation and computational theories of episodic memory, evidence from model organisms suggests that the cornu ammonis 3 (CA3) hippocampal subfield supports recent, but not remote, episodic retrieval. In this study, we demonstrated that recent and remote memories were susceptible to a loss of episodic detail in human participants with focal bilateral damage to CA3. Graph theoretic analyses of 7.0-Tesla resting-state fMRI data revealed that CA3 damage disrupted functional integration across the medial temporal lobe (MTL) subsystem of the default network. The loss of functional integration in MTL subsystem regions was predictive of autobiographical episodic retrieval performance. We conclude that human CA3 is necessary for the retrieval of episodic memories long after their initial acquisition and functional integration of the default network is important for autobiographical episodic memory performance.

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