scholarly journals Directional coupling of slow and fast hippocampal gamma with neocortical alpha/beta oscillations in human episodic memory

2018 ◽  
Author(s):  
Benjamin J. Griffiths ◽  
George Parish ◽  
Frederic Roux ◽  
Sebastian Michelmann ◽  
Mircea van der Plas ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Division Of Labour ◽  
Memory Formation ◽  
Beta Power ◽  
Wide Range ◽  
Directional Coupling ◽  
Alpha Beta ◽  
Episodic Memories ◽  
Flow Of Information

AbstractEpisodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these two processes are thought to be supported by neocortical alpha/beta desynchronisation and hippocampal theta/gamma synchronisation, respectively. Intuitively, these two processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analysing human intracranial EEG data recorded during two associative memory tasks. We find that neocortical alpha/beta (8-20Hz) power decreases reliably precede and predict hippocampal “fast” gamma (60-80Hz) power increases during episodic memory formation; during episodic memory retrieval however, hippocampal “slow” gamma (40-50Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from neocortex to hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.Significance StatementEpisodic memories detail our personally-experienced past. The formation and retrieval of these memories has long been thought to be supported by a division of labour between the neocortex and the hippocampus, where the former processes event-related information and the latter binds this information together. However, it remains unclear how the two regions interact. We uncover directional coupling between these regions, with power decreases in the neocortex that precede and predict power increases in the hippocampus during memory formation. Fascinatingly, this process reverses during memory retrieval, with hippocampal power increases preceding and predicting neocortical power decreases. These results suggest a bidirectional flow of information between the neocortex and hippocampus is fundamental to the formation and retrieval of episodic memories.

scholarly journals Directional coupling of slow and fast hippocampal gamma with neocortical alpha/beta oscillations in human episodic memory

2019 ◽  
Vol 116 (43) ◽  
pp. 21834-21842 ◽  
Author(s):  
Benjamin J. Griffiths ◽  
George Parish ◽  
Frederic Roux ◽  
Sebastian Michelmann ◽  
Mircea van der Plas ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Memory Formation ◽  
Beta Power ◽  
Wide Range ◽  
Alpha Beta ◽  
Episodic Memories ◽  
Hippocampal Theta ◽  
Multisensory Information ◽  
Flow Of Information

Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these 2 processes are thought to be supported by neocortical alpha/beta desynchronization and hippocampal theta/gamma synchronization, respectively. Intuitively, these 2 processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analyzing human intracranial electroencephalogram data recorded during 2 associative memory tasks. We find that neocortical alpha/beta (8 to 20 Hz) power decreases reliably precede and predict hippocampal “fast” gamma (60 to 80 Hz) power increases during episodic memory formation; during episodic memory retrieval, however, hippocampal “slow” gamma (40 to 50 Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from the neocortex to the hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.

scholarly journals Alpha/beta power decreases during episodic memory formation predict the magnitude of alpha/beta power decreases during subsequent retrieval

2021 ◽  
Vol 153 ◽  
pp. 107755
Author(s):  
Benjamin J. Griffiths ◽  
María Carmen Martín-Buro ◽  
Bernhard P. Staresina ◽  
Simon Hanslmayr ◽  
Tobias Staudigl
Keyword(s):  
Episodic Memory ◽  
Memory Formation ◽  
Beta Power ◽  
Alpha Beta

scholarly journals Alpha/beta power decreases during episodic memory formation predict the magnitude of alpha/beta power decreases during subsequent retrieval

2020 ◽  
Author(s):  
Benjamin J. Griffiths ◽  
María Carmen Martín-Buro ◽  
Bernhard P. Staresina ◽  
Simon Hanslmayr ◽  
Tobias Staudigl
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Spectral Power ◽  
Learning Task ◽  
Neural Representation ◽  
Parameter Estimates ◽  
Beta Activity ◽  
Amount Of Information ◽  
Beta Power ◽  
Alpha Beta

AbstractEpisodic memory retrieval is characterised by the vivid reinstatement of information about a personally-experienced event. Growing evidence suggests that the reinstatement of such information is supported by reductions in the spectral power of alpha/beta activity. Given that the amount of information that can be recalled depends on the amount of information that was originally encoded, information-based accounts of alpha/beta activity would suggest that retrieval-related alpha/beta power decreases similarly depend upon decreases in alpha/beta power during encoding. To test this hypothesis, seventeen human participants completed a sequence-learning task while undergoing concurrent MEG recordings. Regression-based analyses were then used to estimate how alpha/beta power decreases during encoding predicted alpha/beta power decreases during retrieval, on a trial-by-trial basis. When subjecting these parameter estimates to group-level analysis, we find evidence to suggest that retrieval-related alpha/beta (7-15Hz) power decreases fluctuate as a function of encoding-related alpha/beta power decreases. These results suggest that retrieval-related alpha/beta power decreases are contingent on the decrease in alpha/beta power that arose during encoding. Subsequent analysis uncovered no evidence to suggest that these alpha/beta power decreases reflect stimulus identity, indicating that the contingency between encoding- and retrieval-related alpha/beta power reflects the reinstatement of a neurophysiological operation, rather than neural representation, during episodic memory retrieval.

scholarly journals Disentangling the roles of neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation

2020 ◽  
Author(s):  
Benjamin J. Griffiths ◽  
María Carmen Martín-Buro ◽  
Bernhard P. Staresina ◽  
Simon Hanslmayr
Keyword(s):  
Episodic Memory ◽  
Memory Performance ◽  
Empirical Support ◽  
Memory Formation ◽  
Information Representation ◽  
Gamma Phase ◽  
Beta Power ◽  
Alpha Beta ◽  
Phase Amplitude ◽  
Hippocampal Theta

AbstractEpisodic memory formation relies on at least two distinct capabilities: 1) our ability to process a vast amount of sensory information, and 2) our ability to bind these sensory representations together to form a coherent memory. The first process is thought to rely on a reduction in neocortical alpha/beta power, while the second is thought to be supported by hippocampal theta-gamma phase-amplitude coupling. However, most studies investigating human episodic memory use paradigms where the two cognitive capabilities overlap. As such, empirical support for the distinction of the two associated neural phenomena is lacking. Here, we addressed this by asking seventeen human participants (11 female, 6 male) to complete a sequence-learning paradigm that temporally separated information representation from mnemonic binding, while MEG recordings were acquired. We found that a decrease in neocortical alpha/beta power during the perception of the sequence correlated with enhanced memory performance. Similar power decreases during mnemonic binding, however, had no bearing on memory formation. In contrast, an increase in hippocampal theta/gamma phase-amplitude coupling during mnemonic binding correlated with enhanced memory performance, but similar coupling during sequence perception bared no relation to later memory performance. These results demonstrate that alpha/beta power decreases and hippocampal theta/gamma phase-amplitude coupling represent two temporally dissociable processes in episodic memory, with the former relating to information representation while the latter relates to mnemonic binding.

scholarly journals Alpha/beta power decreases track the fidelity of stimulus-specific information

2019 ◽  
Author(s):  
Benjamin J. Griffiths ◽  
Stephen D. Mayhew ◽  
Karen J. Mullinger ◽  
João Jorge ◽  
Ian Charest ◽  
...  
Keyword(s):  
Information Processing ◽  
Memory Retrieval ◽  
Negative Relationship ◽  
Memory Task ◽  
Significant Negative Correlation ◽  
Neuronal Firing ◽  
Specific Information ◽  
Beta Power ◽  
Alpha Beta ◽  
Task Irrelevant

AbstractMassed synchronised neuronal firing is detrimental to information processing. When networks of task-irrelevant neurons fire in unison, they mask the signal generated by task-critical neurons. On a macroscopic level, mass synchronisation of these neurons can contribute to the ubiquitous alpha/beta (8-30Hz) oscillations. Reductions in the amplitude of these oscillations, therefore, may reflect a boost in the processing of high-fidelity information within the cortex. Here, we test this hypothesis. Twenty-one participants completed an associative memory task while undergoing simultaneous EEG-fMRI recordings. Using representational similarity analysis, we quantified the amount of stimulus-specific information represented within the BOLD signal on every trial. When correlating this metric with concurrently-recorded alpha/beta power, we found a significant negative correlation which indicated that as alpha/beta power decreased, our metric of stimulus-specific information increased. This effect generalised across cognitive tasks, as the negative relationship could be observed during visual perception and episodic memory retrieval. Further analysis revealed that this effect could be better explained by alpha/beta power decreases providing favourable conditions for information processing, rather than directly representing stimulus-specific information. Together, these results indicate that alpha/beta power decreases parametrically track the fidelity of both externally-presented and internally-generated stimulus-specific information represented within the cortex.

scholarly journals Total recall: episodic memory retrieval, choice, and memory confidence in the rat

2020 ◽  
Author(s):  
Hannah R. Joo ◽  
Hexin Liang ◽  
Jason E Chung ◽  
Charlotte Geaghan-Breiner ◽  
Jiang Lan Fan ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Memory Task ◽  
Correct Choice ◽  
Decision Variable ◽  
Future Behavior ◽  
Episodic Memories ◽  
Past Experiences ◽  
Memory Confidence ◽  
Modern Machine

Episodic memory enables recollection of past experiences to guide future behavior. Humans know which memories to trust (high confidence) and which to doubt (low confidence). How memory retrieval, memory confidence, and memory-guided decisions are related, however, is not understood. Additionally, whether animals can assess confidence in episodic memories to guide behavior is unknown. We developed a spatial episodic memory task in which rats were incentivized to gamble their time: betting more following a correct choice yielded greater reward. Rat behavior reflected memory confidence, with higher temporal bets following correct choices. We applied modern machine learning to identify a memory decision variable, and built a generative model of memories evolving over time that accurately predicted both choices and confidence reports. Our results reveal in rats an ability thought to exist exclusively in primates, and introduce a unified model of memory dynamics, retrieval, choice, and confidence.

scholarly journals Memory for spatio-temporal contextual details during the retrieval of naturalistic episodes

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Samy-Adrien Foudil ◽  
Claire Pleche ◽  
Emiliano Macaluso
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Subjective Experience ◽  
Temporal Order ◽  
Subjective Memory ◽  
Scale Invariant ◽  
Wide Range ◽  
Spatio Temporal ◽  
Invariant Properties ◽  
Context Memory

AbstractEpisodic memory entails the storage of events together with their spatio-temporal context and retrieval comprises the subjective experience of a link between the person who remembers and the episode itself. We used an encoding procedure with mobile-phones to generate experimentally-controlled episodes in the real world: object-images were sent to the participants' phone, with encoding durations up to 3 weeks. In other groups of participants, the same objects were encoded during the exploration of a virtual town (45 min) or using a standard laboratory paradigm, with pairs of object/place-images presented in a sequence of unrelated trials (15 min). At retrieval, we tested subjective memory for the objects (remember/familiar) and memory for the context (place and time). We found that accurate and confident context-memory increased the likelihood of “remember” responses, in all encoding contexts. We also tested the participants' ability to judge the temporal-order of the encoded episodes. Using a model of temporal similarity, we demonstrate scale-invariant properties of order-retrieval, but also highlight the contribution of non-chronological factors. We conclude that the mechanisms governing episodic memory retrieval can operate across a wide range of spatio-temporal contexts and that the multi-dimensional nature of the episodic traces contributes to the subjective experience of retrieval.

scholarly journals Electrophysiological studies of identifying and modulating the preparatory strategic processes involved in episodic memory retrieval

2018 ◽  
Author(s):  
◽  
Mason H. Price
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Task Demands ◽  
Event Related Potential ◽  
Oscillatory Activity ◽  
Retrieval Task ◽  
Retrieval Cues ◽  
Starting Point ◽  
Episodic Memories ◽  
Cue Processing

Successful retrieval of episodic memories has been shown to depend on the overlap between the processes engaged during encoding and those re-engaged during retrieval. The ability to strategically adapt cue processing to maximize this overlap, sometimes referred to as “retrieval orientation”, has been supported by numerous studies employing electroencephalography (EEG), which demonstrate differences according to the class of memories being sought. However, research in this domain has largely focused on event-related potential (ERP) effects of sustained amplitude that occur after the onset of retrieval cues, thereby failing to indicate whether such effects might be engaged in a preparatory manner before cue onset. Here, we describe two experiments that addressed this issue by employing an analysis approach focusing on the pre-stimulus period of retrieval test trials and capitalizing on the increased sensitivity of multivariate pattern analysis (MVPA) of oscillatory activity. Experiment 1 established evidence of a preparatory form of retrieval orienting and examined the potential fluctuation versus stability of such processing. Experiment 2 attempted to directly modulate the engagement of orienting processes by parametrically manipulating the extent to which responses during the retrieval task are speeded. By novelly quantifying the relationship between multivariate neural correlates of retrieval orientation and behavioral measures of performance, and testing how orienting might be flexibly adjusted to meet task demands, the current project serves as a starting point for developing techniques aimed at improving episodic memory retrieval through strategic control.

scholarly journals Hippocampal-cortical encoding activity predicts the precision of episodic memory

2020 ◽  
Author(s):  
Saana M. Korkki ◽  
Franziska R. Richter ◽  
Jon S. Simons
Keyword(s):  
Episodic Memory ◽  
Memory Retrieval ◽  
Neural Substrates ◽  
Memory Formation ◽  
Continuous Scale ◽  
Neuroimaging Data ◽  
Memory Representations ◽  
Past Experiences ◽  
Object Features ◽  
Memory Precision

AbstractOur recollections of past experiences can vary both in the number of specific event details accessible from memory and the precision with which such details are reconstructed. Prior neuroimaging evidence suggests the success and precision of episodic recollection to rely on distinct neural substrates during memory retrieval. In contrast, the specific encoding mechanisms supporting later memory precision, and whether they differ from those underlying successful memory formation in general, are currently unknown. Here, we combined continuous measures of memory retrieval with model-based analyses of behavioural and neuroimaging data to tease apart the encoding correlates of successful memory formation and mnemonic precision. In the MRI scanner, participants encoded object-scene displays, and later reconstructed features of studied objects using a continuous scale. We observed overlapping encoding activity in inferior prefrontal and posterior perceptual regions to predict both which object features were later remembered versus forgotten, and the precision with which they were reconstructed from memory. In contrast, hippocampal encoding activity significantly predicted the precision, but not overall success, of subsequent memory retrieval. The current results identify a hippocampal-cortical encoding basis for episodic memory precision, and suggest a contribution of shared cortical encoding mechanisms to the formation of both accessible and precise memory representations.

scholarly journals Brain oscillations track the formation of episodic memories in the real world

2016 ◽  
Author(s):  
Benjamin Griffiths ◽  
Ali Mazaheri ◽  
Stefan Debener ◽  
Simon Hanslmayr
Keyword(s):  
Episodic Memory ◽  
Real World ◽  
Medial Temporal Lobe ◽  
Spatial Clustering ◽  
Inferior Frontal Gyrus ◽  
Low Frequency ◽  
Blind Spot ◽  
Memory Formation ◽  
The Real ◽  
Beta Power

Despite the well-known influence of environmental context on episodic memory, little has been done to enhance contextual richness within the lab. This leaves a blind spot lingering over the neuronal correlates of episodic memory formation in the real world. To address this, we presented participants with series of words to memorise along a pre-designated route across campus. Meanwhile, a mobile EEG system acquired the associated neural activity. Replicating lab-based subsequent memory effects (SMEs), we identified significant low-frequency power decreases, including beta power decreases over the left inferior frontal gyrus. Additionally, the paradigm enabled us to dissociate the oscillatory correlates of temporal and spatial clustering. Specifically, we found spatially clustered items exhibited significantly greater theta power decreases within the left medial temporal lobe than temporally clustered items. These findings go beyond lab-based studies, which are limited in their capabilities to investigate environmental contextual factors that guide memory formation.

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