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

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.

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

10.1101/2020.01.22.915330 ◽

2020 ◽

Cited By ~ 1

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.

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

10.1101/305698 ◽

2018 ◽

Cited By ~ 2

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.

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

10.1101/2020.07.08.193763 ◽

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.

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Disentangling neocortical alpha/beta and hippocampal theta/gamma oscillations in human episodic memory formation

NeuroImage ◽

10.1016/j.neuroimage.2021.118454 ◽

2021 ◽

pp. 118454

Author(s):

Benjamin J. Griffiths ◽

María Carmen Martín-Buro ◽

Bernhard P. Staresina ◽

Simon Hanslmayr

Keyword(s):

Episodic Memory ◽

Gamma Oscillations ◽

Memory Formation ◽

Alpha Beta ◽

Hippocampal Theta

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

10.1101/042929 ◽

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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Knowledge is power: prior knowledge aids memory formation for both congruent and incongruent events, but in different ways.

10.31234/osf.io/um4ga ◽

2017 ◽

Author(s):

Andrea Greve ◽

Elisa Cooper ◽

Roni Tibon ◽

Richard Henson

Keyword(s):

Episodic Memory ◽

Prior Knowledge ◽

Memory Performance ◽

Memory Formation ◽

Memory Test ◽

World Knowledge ◽

Apparent Paradox ◽

Power Prior

Events that conform to our expectations, i.e, are congruent with our world knowledge or schemas, are better remembered than unrelated events. Yet events that conflict with schemas can also be remembered better. We examined this apparent paradox in four experiments, in which schemas were established by training ordinal relationships between randomly-paired objects, while episodic memory was tested for the number of objects on each trial. Better memory was found for both congruent and incongruent trials, relative to unrelated trials, producing memory performance that was a “U-shaped” function of congruency. Furthermore, the incongruency advantage, but not congruency advantage, emerged even if the information probed by the memory test was irrelevant to the schema, while the congruency advantage, but not incongruency advantage, also emerged after initial encoding. Schemas therefore augment episodic memory in multiple ways, depending on the match between novel and existing information.

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Cognitive processes supporting episodic memory formation in childhood: The role of source memory, binding, and executive functioning

Developmental Review ◽

10.1016/j.dr.2011.02.001 ◽

2010 ◽

Vol 30 (4) ◽

pp. 384-402 ◽

Cited By ~ 42

Author(s):

Vinaya Raj ◽

Martha Ann Bell

Keyword(s):

Executive Functioning ◽

Episodic Memory ◽

Cognitive Processes ◽

Source Memory ◽

Memory Formation ◽

Memory Binding

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On the Effectiveness of Event-related Beta tACS on Episodic Memory Formation and Motor Cortex Excitability

10.1101/078964 ◽

2016 ◽

Cited By ~ 1

Author(s):

Verena Braun ◽

Rodika Sokoliuk ◽

Simon Hanslmayr

Keyword(s):

Motor Cortex ◽

Episodic Memory ◽

Inferior Frontal Gyrus ◽

Memory Formation ◽

Frequency Range ◽

Beta Oscillations ◽

Healthy Human ◽

Sham Stimulation ◽

Motor Cortex Excitability ◽

Beta Frequency

AbstractBackgroundTranscranial alternating current stimulation (tACS) is widely used to entrain or modulate brain oscillations in order to investigate causal relationships between oscillations and cognition.ObjectiveIn a series of experiments we here addressed the question of whether event-related, transient tACS in the beta frequency range can be used to entrain beta oscillations in two different domains: episodic memory formation and motor cortex excitability.MethodsIn experiments 1 and 2, 72 healthy human participants engaged in an incidental encoding task of verbal and non-verbal material while receiving tACS to the left and right inferior frontal gyrus (IFG) at 6.8Hz, 10.7Hz, 18.5Hz, 30Hz, 48Hz and sham stimulation for 2s during stimulus presentation.In experiment 3, tACS was administered to M1 at the individual motor beta frequency of eight subjects. We investigated the relationship between the size of TMS induced MEPs and tACS phase.ResultsBeta tACS did not affect memory performance compared to sham stimulation in experiments 1 and 2. Likewise, in experiment 3, MEP size was not modulated by the tACS phase.ConclusionsOur findings suggest that event-related, transient tACS in the beta frequency range cannot be used to modulate the formation of episodic memories or motor cortex excitability. These null-results question the effectiveness of event-related tACS to entrain beta oscillations and modulate cognition.

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

10.1101/633107 ◽

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.

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