Similar patterns of neural activity predict memory function during encoding and retrieval

Kragel, James E.; Ezzyat, Youssef; Sperling, Michael R.; Gorniak, Richard; Worrell, Gregory A.; Berry, Brent M.; Inman, Cory S.; Lin, Jui-Jui; Davis, Kathryn A.; Das, Sandhitsu R.; Stein, Joel M.; Jobst, Barbara C.; Zaghloul, Kareem A.; Sheth, Sameer A.; Rizzuto, Daniel S.; Kahana, Michael J.

doi:10.1016/j.neuroimage.2017.03.042

Cited by 61 publications

(62 citation statements)

References 78 publications

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“…They thereby specifically indicate a role for theta 277 oscillations in retrieving items that are accompanied, organized and cued by their encoding 278 context. Our results might initially seem at odds with studies observing a spectral tilt with increased 279 high-frequency power and decreased low-frequency power leading up to successful recall 280 compared to deliberation [29][30][31][32]. At a closer look, they seem to indicate that a more strongly 281 matched recall contrast (such as recall with vs. without contextual information) reveals a neural 282 signature of associative retrieval that is often hidden under a global spectral tilt, which may, in 283 turn, relate to more general activation/attention processes accompanying recall.…”

Section: Retrieval 270mentioning

confidence: 71%

“…Theta oscillations have 72 been suggested to support the formation of both spatial and episodic associations by organizing 73 spike-timing and associated plasticity [28], but evidence in favor of this idea is scarce. In fact, 74 successful episodic memory operations are often associated with a wide-spread decrease in low-75 and increase in high-frequency power [29][30][31][32]. Despite such broad-band tilt effects, however, more 76 localized increases in temporal narrow-band theta oscillations during successful encoding [33] and 77 retrieval [30,31] also exist.…”

Section: Introduction 37mentioning

confidence: 99%

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Reactivated spatial context guides episodic recall

Herweg

Sharan

Sperling

et al. 2018

Preprint

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25The medial temporal lobe (MTL) is known as the locus of spatial coding and episodic memory, 26 but the interaction between these cognitive domains, as well as the extent to which they rely on 27 common neurophysiological mechanisms is poorly understood. Here, we use a hybrid spatial-28 episodic memory task to determine how spatial information is dynamically reactivated in sub-29 regions of the MTL and how this reactivation guides recall of episodic information. Our results 30 implicate theta oscillations across the MTL as a common neurophysiological substrate for spatial 31 coding in navigation and episodic recall. We further show that spatial context information is 32 initially retrieved in the hippocampus (HC) and subsequently emerges in the parahippocampal 33 gyrus (PHG). Finally, we demonstrate that hippocampal theta phase modulates parahippocampal 34 gamma amplitude during retrieval of spatial context, suggesting a role for cross frequency coupling 35 in coding and transmitting retrieved spatial information. 36

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Section: Retrieval 270mentioning

confidence: 71%

Section: Introduction 37mentioning

confidence: 99%

Reactivated spatial context guides episodic recall

Herweg

Sharan

Sperling

et al. 2018

Preprint

Self Cite

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“…Second, we examined a memory retrieval contrast, wherein epochs of time leading up to verbalization of a recalled item are compared to matched epochs of time, from other word lists, where no recall occurs (e.g. 29,40,41; see Methods for details). We refer to these matched periods as "deliberation" intervals.…”

Section: Resultsmentioning

confidence: 99%

“…In this way, we aimed to contrast activity related to successful retrieval against activity during which subjects were liable to try, but fail, to recall a word. This paradigm has been employed in several prior studies examining the neural correlates of free recall (3,29,41,40). However, free-recall tasks inherently confound neural process responsible for episodic retrieval with processes responsible for vocalization and motor preparatory behavior.…”

Section: Discussionmentioning

confidence: 99%

Functional wiring of the human medial temporal lobe

Solomon

Stein

Das

et al. 2018

Preprint

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The medial temporal lobe (MTL) is a locus of episodic memory in the human brain. It is comprised of cytologically distinct subregions that, in concert, give rise to successful encoding and retrieval of context-dependent memories. However, the functional connections between these subregions are poorly understood. To determine functional connectivity among MTL subregions, we had 108 subjects fitted with indwelling electrodes perform a verbal episodic memory task, and asked how encoding or retrieval correlated with coherence between regions.Here we report that coherent theta (4-8 Hz) activity underlies successful episodic memory, whereas high-frequencies exhibit significant desynchronization. During encoding, theta connections converge on the left entorhinal cortex, which concurrently exhibits an increase in high-frequency spectral power. Perirhinal cortex emerges as a hub of retrieval-associated theta connectivity, reflecting a substantial reorganization of the encoding-associated network. We

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“…Subsequently, anatomic localization of bipolar pairs (computed as the mid-point between the two contacts) was accomplished using 2 independent processing pipelines for depth and surface electrodes which were later transformed to MNI space similar to previous studies (Burke JF et al, 2013;Kragel JE et al, 2017).…”

Section: Figure 1 ^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^^mentioning

confidence: 99%

Tonic resting-state hubness supports high-frequency activity defined verbal-memory encoding network in epilepsy

Chaitanya

Hinds

Kragel

et al. 2019

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High-frequency gamma activity of verbal-memory encoding using invasive-electroencephalogram coupled has laid the foundation for numerous studies testing the integrity of memory in diseased populations. Yet, the functional connectivity characteristics of networks subserving these HFAmemory linkages remains uncertain. By integrating this electrophysiological biomarker of memory encoding from IEEG with resting-state BOLD fluctuations, we estimated the segregation and hubness of HFA-memory regions in drug-resistant epilepsy patients and matched healthy controls. HFA-memory regions express distinctly different hubness compared to neighboring regions in health and in epilepsy, and this hubness was more relevant than segregation in predicting verbal memory encoding. The HFA-memory network comprised regions from both the cognitive control and primary processing networks, validating that effective verbal-memory encoding requires multiple functions, and is not dominated by a central cognitive core. Our results demonstrate a tonic intrinsic set of functional connectivity, which provides the necessary conditions for effective, phasic, task-dependent memory encoding. AbbreviationsHFA -High-frequency activity MEM -Brain regions showing HFA associated with verbal-memory encoding CN -Controls Nodes P.REC -Percentage of words recalled during IEEG memory testing CVLT -California Verbal Learning Test IEEG -Invasive Electroencephalography BC -Betweenness Centrality CC-Clustering Coefficient PC -Participation Coefficient Highlights 1. High frequency memory activity in IEEG corresponds to specific BOLD changes in resting-state data.2. HFA-memory regions had lower hubness relative to control brain nodes in both epilepsy patients and healthy controls.3. HFA-memory network displayed hubness and participation (interaction) values distinct from other cognitive networks.4. HFA-memory network shared regional membership and interacted with other cognitive networks for successful memory encoding. 5. HFA-memory network hubness predicted both concurrent task (phasic) and baseline (tonic) verbal-memory encoding success.resting-state fMRI (rsfMRI) data to characterize the network architecture of a task-defined HFAmemory network and understand its relationship to the functional connectivity of a broader set of intrinsic resting-state networks. Graph theory has been a useful tool for mapping functional networks and characterizing their properties during task and at rest. Three important graph indices that are essential in characterizing brain regions and their functionality include: (1) clustering coefficient (CC), which captures network segregation and local information processing and (2) betweenness centrality (BC), which captures hubness and the degree of importance held by a region that connects two or more modules and (3) participation coefficient (PC) which measures the extent to which regions within a network connect to networks other than its own, with a higher participation coefficient indicating that the regions connect with a variety of o...

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Similar patterns of neural activity predict memory function during encoding and retrieval

Cited by 61 publications

References 78 publications

Reactivated spatial context guides episodic recall

Reactivated spatial context guides episodic recall

Functional wiring of the human medial temporal lobe

Tonic resting-state hubness supports high-frequency activity defined verbal-memory encoding network in epilepsy

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