scholarly journals Increased task-dependent functional connectivity by stimulation of the hippocampal network predicts memory enhancement

2019 ◽  
Author(s):  
Kristen N. Warren ◽  
Molly S. Hermiller ◽  
Aneesha S. Nilakantan ◽  
Joel L. Voss
Keyword(s):  
Functional Connectivity ◽  
Episodic Memory ◽  
Memory Retrieval ◽  
Medial Temporal Lobe ◽  
Network Connectivity ◽  
Network Control ◽  
Retrieval Task ◽  
Memory Processing ◽  
Hippocampal Network ◽  
Hippocampal Networks

AbstractSuccessful episodic memory involves dynamic increases in the coordination of activity across distributed hippocampal networks, including the posterior-medial network (PMN) and the anterior-temporal network (ATN). We tested whether this up-regulation of functional connectivity during memory processing can be enhanced within hippocampal networks by noninvasive stimulation, and whether such task-dependent connectivity enhancement predicts episodic memory improvement. Participants received stimulation targeting either the PMN or an out-of-network control location. We compared the effects of stimulation on fMRI connectivity measured during an autobiographical memory retrieval task versus during rest within the PMN and the ATN. PMN-targeted stimulation significantly increased connectivity during memory retrieval versus rest within the PMN. This effect was not observed in the ATN, or in either network due to control out-of-network stimulation. Task-dependent increases in connectivity due to PMN-targeted stimulation within the medial temporal lobe predicted improved performance of a separate episodic memory test. It is therefore possible to enhance the task-dependent regulation of hippocampal network connectivity that supports memory processing using noninvasive stimulation.

scholarly journals Stimulating the hippocampal posterior-medial network enhances task-dependent connectivity and memory

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Kristen N Warren ◽  
Molly S Hermiller ◽  
Aneesha S Nilakantan ◽  
Joel L Voss
Keyword(s):  
Episodic Memory ◽  
Medial Temporal Lobe ◽  
Network Connectivity ◽  
Network Control ◽  
Retrieval Task ◽  
Memory Processing ◽  
Hippocampal Network ◽  
Improved Performance ◽  
Hippocampal Networks ◽  
Control Stimulation

Successful episodic memory involves dynamic increases in activity across distributed hippocampal networks, including the posterior-medial (PMN) and the anterior-temporal (ATN) networks. We tested whether this up-regulation of functional connectivity during memory processing can be enhanced within hippocampal networks by noninvasive stimulation, and whether such task-dependent connectivity enhancement predicts memory improvement. Participants received stimulation targeting the PMN or an out-of-network control location. We compared the effects of stimulation on fMRI connectivity during an autobiographical retrieval task versus during rest within the PMN and the ATN. PMN-targeted stimulation significantly increased connectivity during autobiographical retrieval versus rest within the PMN. This effect was not observed in the ATN, or in either network following control stimulation. Task-dependent increases in connectivity within the medial temporal lobe predicted improved performance of a separate episodic memory test. It is therefore possible to enhance the task-dependent regulation of hippocampal network connectivity that supports memory processing using noninvasive stimulation.

scholarly journals Functional wiring of the human medial temporal lobe

2018 ◽  
Author(s):  
E. A. Solomon ◽  
J. M. Stein ◽  
S. Das ◽  
R. Gorniak ◽  
M. R. Sperling ◽  
...  
Keyword(s):  
Functional Connectivity ◽  
Episodic Memory ◽  
Temporal Lobe ◽  
Medial Temporal Lobe ◽  
Memory Task ◽  
Memory Processing ◽  
High Frequencies ◽  
Functional Connections ◽  
Brain Functions ◽  
Encoding And Retrieval

AbstractThe 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 126 subjects fitted with indwelling electrodes perform a verbal memory task, and asked how encoding or retrieval correlated with interregional synchronization. Using phase-based measures of connectivity, we found that synchronous theta (4-8 Hz) activity underlies successful episodic memory, whereas high-frequencies exhibit desynchronization. Moreover, theta functional connectivity during encoding aligned with key anatomic connections, including critical links between the entorhinal cortex, dentate gyrus, and CA1 of the hippocampus. Retrieval-associated networks demonstrated enhanced involvement of the subiculum, reflecting a substantial reorganization of the encoding-associated network. We posit that coherent theta activity within the MTL marks periods of successful memory, but distinct patterns of connectivity dissociate key stages of memory processing.Significance StatementThe brain functions through the interaction of its distinct parts, but little is known about how such connectivity dynamics relate to learning and memory. We used a large dataset of 126 human subjects with intracranial electrodes to assess patterns of electrical connectivity within the medial temporal lobe – a key region for memory processing – as they performed a memory task. We discovered that unique networks of time-varying, low-frequency interactions correlate with memory encoding and retrieval, specifically in the theta band. Simultaneously, we observed elevated spectral power at high frequencies in these same regions. The result is a complete map of physiological dynamics within the MTL, highlighting how a reorganization of theta networks support distinct memory operations.

Going Their Separate Ways: Dissociation of Hippocampal and Dorsolateral Prefrontal Activation during Episodic Retrieval and Post-retrieval Processing

2010 ◽  
Vol 22 (3) ◽  
pp. 513-525 ◽  
Author(s):  
Sarah L. Israel ◽  
Tyler M. Seibert ◽  
Michelle L. Black ◽  
James B. Brewer
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Relative Increase ◽  
Network Activity ◽  
Default Network ◽  
Episodic Retrieval ◽  
Retrieval Task ◽  
Paired Associates ◽  
Hippocampal Activity ◽  
Dorsolateral Prefrontal

Hippocampal activity is modulated during episodic memory retrieval. Most consistently, a relative increase in activity during confident retrieval is observed. Dorsolateral prefrontal cortex (DLPFC) is also activated during retrieval, but may be more generally activated during cognitive-control processes. The “default network,” regions activated during rest or internally focused tasks, includes the hippocampus, but not DLPFC. Therefore, DLPFC and the hippocampus should diverge during difficult tasks suppressing the default network. It is unclear, however, whether a difficult episodic memory retrieval task would suppress the default network due to difficulty or activate it due to internally directed attention. We hypothesized that a task requiring episodic retrieval followed by rumination on the retrieved item would increase DLPFC activity, but paradoxically reduce hippocampal activity due to concomitant suppression of the default network. In the present study, blocked and event-related fMRI were used to examine hippocampal activity during episodic memory recollection and postretrieval processing of paired associates. Subjects were asked to make living/nonliving judgments about items visually presented (classify) or items retrieved from memory (recall–classify). Active and passive baselines were used to differentiate task-related activity from default-network activity. During the “recall–classify” task, anterior hippocampal activity was selectively reduced relative to “classify” and baseline tasks, and this activity was inversely correlated with DLPFC. Reaction time was positively correlated with DLPFC activation and default-network/hippocampal suppression. The findings demonstrate that frontal and hippocampal activity are dissociated during difficult episodic retrieval tasks and reveal important considerations for interpreting hippocampal activity associated with successful episodic retrieval.

Lateralization of Prefrontal Activity during Episodic Memory Retrieval: Evidence for the Production-Monitoring Hypothesis

2003 ◽  
Vol 15 (2) ◽  
pp. 249-259 ◽  
Author(s):  
Roberto Cabeza ◽  
Jill K. Locantore ◽  
Nicole D. Anderson
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Medial Temporal Lobe ◽  
Item Recognition ◽  
Cued Recall ◽  
Anterior Cingulate ◽  
Episodic Retrieval ◽  
Context Recognition ◽  
Production Monitoring ◽  
The Right

We propose a new hypothesis concerning the lateralization of prefrontal cortex (PFC) activity during verbal episodic memory retrieval. The hypothesis states that the left PFC is differentially more involved in semantically guided information production than is the right PFC, and that the right PFC is differentially more involved in monitoring and verification than is the left PFC. This “production-monitoring hypothesis” differs from the existing “systematic-heuristic hypothesis,” which proposes that the left PFC is primarily involved in systematic retrieval operations, and the right PFC in heuristic retrieval operations. To compare the two hypotheses, we measured PFC activity using positron emission tomography (PET) during the performance of four episodic retrieval tasks: stem cued recall, associative cued recall, context recognition (source memory), and item recognition. Recall tasks emphasized production processes, whereas recognition tasks emphasized monitoring processes. Stem cued recall and context-recognition tasks underscored systematic operations, whereas associative cued recall and item-recognition tasks underscored heuristic operations. Consistent with the production-monitoring hypothesis, the left PFC was more activated for recall than for recognition tasks and the right PFC was more activated for recognition than for recall tasks. Inconsistent with the systematic-heuristic hypothesis, the left PFC was more activated for heuristic than for systematic tasks and the right PFC showed the converse result. Additionally, the study yielded activation differences outside the PFC. In agreement with a previous recall/recognition PET study, anterior cingulate, cerebellar, and striatal regions were more activated for recall than for recognition tasks, and the converse occurred for posterior parietal regions. A right medial temporal lobe region was more activated for stem cued recall and context recognition than for associative cued recall and item recognition, possibly reflecting perceptual integration. In sum, the results provide evidence for the production-monitoring hypothesis and clarify the role of different brain regions typically activated in PET and functional magnetic resonance imaging (fMRI) studies of episodic retrieval.

scholarly journals Age-Related Compensatory Reconfiguration of PFC Connections during Episodic Memory Retrieval

2020 ◽  
Author(s):  
Lifu Deng ◽  
Mathew L Stanley ◽  
Zachary A Monge ◽  
Erik A Wing ◽  
Benjamin R Geib ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Medial Temporal Lobe ◽  
Memory Performance ◽  
Functional Integration ◽  
Brain Network ◽  
Age Related ◽  
Connectivity Patterns ◽  
The Brain ◽  
Related Increase

Abstract During demanding cognitive tasks, older adults (OAs) frequently show greater prefrontal cortex (PFC) activity than younger adults (YAs). This age-related increase in PFC activity is often associated with enhanced cognitive performance, suggesting functional compensation. However, the brain is a complex network of interconnected regions, and it is unclear how network connectivity of PFC regions differs for OAs versus YAs. To investigate this, we examined the age-related difference on the functional brain networks mediating episodic memory retrieval. YAs and OAs participants encoded and recalled visual scenes, and age-related differences in network topology during memory retrieval were investigated as a function of memory performance. We measured both changes in functional integration and reconfiguration in connectivity patterns. The study yielded three main findings. First, PFC regions were more functionally integrated with the rest of the brain network in OAs. Critically, this age-related increase in PFC integration was associated with better retrieval performance. Second, PFC regions showed stronger performance-related reconfiguration of connectivity patterns in OAs. Finally, the PFC reconfiguration increases in OAs tracked reconfiguration reductions in the medial temporal lobe (MTL)—a core episodic memory region, suggesting that PFC connectivity in OAs may be compensating for MTL deficits.

scholarly journals Prefrontal, striatal, and VTA subnetwork dynamics during novelty and exploration

2021 ◽  
Author(s):  
Adam JO Dede ◽  
Nader Marzban ◽  
Ashutosh Mishra ◽  
Robert Reichert ◽  
Paul M Anderson ◽  
...  
Keyword(s):  
Time Series ◽  
Functional Connectivity ◽  
Information Exchange ◽  
Network Connectivity ◽  
Baseline Period ◽  
Male Rats ◽  
Memory Processing ◽  
Delta Band ◽  
Eigen Decomposition ◽  
Regional Clustering

Multiple distinct brain areas have been implicated in memory including the prefrontal cortex (PFC), striatum (STR), and ventral tegmental area (VTA). Information-exchange across these widespread networks requires flexible coordination at a fine time-scale. In the present study, we collected high-density recordings from the PFC, STR, and VTA of male rats during baseline, encoding, consolidation, and retrieval stages of memory formation. Novel sub-regional clustering analyses identified patterns of spatially restricted, temporally coherent, and frequency specific signals that were reproducible across days and were modulated by behavioral states. Clustering identified miniscule patches of neural tissue. Generalized eigen decomposition (GED) reduced each cluster to a single time series. Amplitude envelope correlation of the cluster time series was used to assess functional connectivity between clusters. Dense intra- and inter regional functional connectivity characterized the baseline period, with delta oscillations playing an outsized role. There was a dramatic pruning of network connectivity during encoding. Connectivity rebounded during consolidation, but connections in the theta band became stronger, and those in the delta band were weaker. Finally, during retrieval, connections were not as severely reduced as they had been during encoding, and specifically theta and higher-frequency connections were stronger. Underlying these connectivity changes, the anatomical extent of clusters observed in the gamma band in the PFC and in both the gamma and delta bands in the VTA changed markedly across behavioral conditions. These results demonstrate the brain's ability to reorganize functionally at both the intra- and inter-regional levels during different stages of memory processing.

scholarly journals Evidence for immediate enhancement of hippocampal memory encoding by network-targeted theta-burst stimulation during concurrent fMRI

2020 ◽  
Author(s):  
Molly S. Hermiller ◽  
Yu Fen Chen ◽  
Todd B. Parrish ◽  
Joel L. Voss
Keyword(s):  
Episodic Memory ◽  
Neural Activity ◽  
Theta Band ◽  
Theta Burst Stimulation ◽  
Burst Stimulation ◽  
Related Activity ◽  
Memory Processing ◽  
Hippocampal Activity ◽  
Hippocampal Network ◽  
Theta Burst

AbstractThe hippocampus supports episodic memory via interaction with a distributed brain network. Previous experiments using network-targeted noninvasive brain stimulation have identified episodic memory enhancements and modulation of activity within the hippocampal network. However, mechanistic insights were limited because these effects were measured long after stimulation and therefore could have reflected various neuroplastic aftereffects with extended timecourses. In this experiment with human subjects of both sexes, we tested for immediate stimulation impact on encoding-related activity of the hippocampus and immediately adjacent medial-temporal cortex by delivering theta-burst transcranial magnetic stimulation (TBS) concurrent with fMRI, as an immediate impact of stimulation would suggest an influence on neural activity. We reasoned that TBS would be particularly effective for influencing the hippocampus because rhythmic neural activity in the theta band is associated with hippocampal memory processing. First, we demonstrated that it is possible to obtain robust fMRI correlates of task-related activity during concurrent TBS. We then identified immediate effects of TBS on encoding of visual scenes. Brief volleys of TBS targeting the hippocampal network increased activity of the targeted (left) hippocampus during scene encoding and increased subsequent recollection. Stimulation did not influence activity during an intermixed numerical task with no memory demand. Control conditions using beta-band and out-of-network stimulation also did not influence hippocampal activity or recollection. TBS targeting the hippocampal network therefore immediately impacted hippocampal memory processing. This suggests direct, beneficial influence of stimulation on hippocampal neural activity related to memory and supports the role of theta-band activity in human episodic memory.Significance StatementCan noninvasive stimulation directly impact function of indirect, deep-brain targets such as the hippocampus? We tested this by targeting an accessible region of the hippocampal network via transcranial magnetic stimulation during concurrent fMRI. We reasoned that theta-burst stimulation would be particularly effective for impacting hippocampal function, as this stimulation rhythm should resonate with the endogenous theta-nested-gamma activity prominent in hippocampus. Indeed, theta-burst stimulation targeting the hippocampal network immediately impacted hippocampal activity during encoding, improving memory formation as indicated by enhanced later recollection. Rhythm- and location-control stimulation conditions had no such effects. These findings suggest a direct influence of noninvasive stimulation on hippocampal neural activity and highlight that the theta-burst rhythm is relatively privileged in its ability to influence hippocampal memory function.

scholarly journals The neural dynamics of novel scene imagery

2018 ◽  
Author(s):  
Daniel N. Barry ◽  
Gareth R. Barnes ◽  
Ian A. Clark ◽  
Eleanor A. Maguire
Keyword(s):  
Prefrontal Cortex ◽  
Episodic Memory ◽  
Temporal Resolution ◽  
Memory Retrieval ◽  
Brain Regions ◽  
Ventromedial Prefrontal Cortex ◽  
Neural Dynamics ◽  
High Temporal Resolution ◽  
Memory Processing ◽  
Crucial Component

AbstractRetrieval of long-term episodic memories is characterised by synchronised neural activity between hippocampus and ventromedial prefrontal cortex (vmPFC), with additional evidence that vmPFC activity leads that of the hippocampus. It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. If this is the case, then a comparable interaction between the two brain regions should exist during the construction of novel scene imagery. To address this question, we leveraged the high temporal resolution of magnetoencephalography (MEG) to investigate the construction of novel mental imagery. We tasked male and female humans with imagining scenes and single isolated objects in response to one-word cues. We performed source level power, coherence and causality analyses to characterise the underlying inter-regional interactions. Both scene and object imagination resulted in theta power changes in the anterior hippocampus. However, higher theta coherence was observed between the hippocampus and vmPFC in the scene compared to the object condition. This inter-regional theta coherence also predicted whether or not imagined scenes were subsequently remembered. Dynamic causal modelling of this interaction revealed that vmPFC drove activity in hippocampus during novel scene construction. Additionally, theta power changes in the vmPFC preceded those observed in the hippocampus. These results constitute the first evidence in humans that episodic memory retrieval and scene imagination rely on similar vmPFC-hippocampus neural dynamics. Furthermore, they provide support for theories emphasising similarities between both cognitive processes, and perspectives that propose the vmPFC guides the construction of context-relevant representations in the hippocampus.Significance statementEpisodic memory retrieval is characterised by a dialogue between hippocampus and ventromedial prefrontal cortex (vmPFC). It has been proposed that the mental generation of scene imagery is a crucial component of episodic memory processing. An ensuing prediction would be of a comparable interaction between the two brain regions during the construction of novel scene imagery. Here, we leveraged the high temporal resolution of magnetoencephalography (MEG), and combined it with a scene imagination task. We found that a hippocampal-vmPFC dialogue existed, and that it took the form of vmPFC driving the hippocampus. We conclude that episodic memory and scene imagination share fundamental neural dynamics, and the process of constructing vivid, spatially coherent, contextually appropriate scene imagery is strongly modulated by vmPFC.

scholarly journals Multiple parietal pathways are associated with rTMS-induced hippocampal network enhancement and episodic memory changes

2020 ◽  
Author(s):  
Michael Freedberg ◽  
Catherine A. Cunningham ◽  
Cynthia M. Fioriti ◽  
Jorge Dorado Murillo ◽  
Jack A. Reeves ◽  
...  
Keyword(s):  
Individual Differences ◽  
Episodic Memory ◽  
Medial Temporal Lobe ◽  
Diffusion Tensor ◽  
Repetitive Transcranial Magnetic Stimulation ◽  
Procedural Memory ◽  
Resting State Functional Connectivity ◽  
Parahippocampal Cortex ◽  
Inferior Parietal Cortex ◽  
Hippocampal Network

AbstractRepetitive transcranial magnetic stimulation (rTMS) of the inferior parietal cortex (IPC) increases resting-state functional connectivity (rsFC) of the hippocampus with the precuneus and other posterior cortical areas and causes proportional improvement of episodic memory. The anatomical pathway responsible for the propagation of these effects from the IPC is unknown and may not be direct. Using diffusion tensor imaging, we examined whether individual differences in fractional anisotropy (FA), a tensor-derived quantity related to white matter properties, in pathways between the IPC and medial temporal lobe (MTL), via the parahippocampal cortex and the precuneus, accounted for individual differences in hippocampal rsFC and memory change after rTMS. FA in the IPC-parahippocampal pathway was associated with rsFC change in a few small cortical clusters, while FA in the IPC-precuneus pathway was strongly linked to widespread changes in rsFC. FA in both pathways was related to episodic memory, but not to procedural memory. These results implicate pathways to the MTL and to the precuneus in the enhancing effect of parietal rTMS on hippocampal rsFC and memory.

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