scholarly journals Hippocampal theta oscillations support successful associative memory formation

2020 ◽  
Author(s):  
Srinivas Kota ◽  
Michael D. Rugg ◽  
Bradley C. Lega
Keyword(s):  
Associative Memory ◽  
Memory Formation ◽  
Associative Recognition ◽  
Theta Oscillations ◽  
Memory Encoding ◽  
Phase Reset ◽  
Intracranial Eeg ◽  
Electrophysiological Evidence ◽  
Hippocampal Theta ◽  
Encoding And Retrieval

1.AbstractModels of memory formation posit that recollection as compared to familiarity-based memory depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected versus those that are recognized on the basis of familiarity should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans results have not been as clear. Here, we employed an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients undergoing intracranial EEG monitoring. We identified a dissociation between 2– 5 Hz and 5–9 Hz theta oscillations, by which 2–5 Hz oscillations uniquely were linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding, distinguished recollected from familiar items at retrieval, and contributed to reinstatement of encoding-related patterns that distinguished these items. Our results provide direct electrophysiological evidence that 2–5 Hz hippocampal theta oscillations support the encoding and retrieval of memories based on recollection but not familiarity.2.Significance StatementExtensive fMRI evidence suggests that the hippocampus plays a selective role in recollection rather than familiarity, during both encoding and retrieval. However, there is little or no electrophysiological evidence that speaks to whether the hippocampus is selectively involved in recollection. Here, we used intracranial EEG from human participants engaged in an associative recognition paradigm. The findings suggest that oscillatory power and phase reset in the hippocampus are selectively associated with recollection rather than familiarity-based memory judgements. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection than familiarity. Collectively, the findings support a role for hippocampal theta oscillations in human episodic memory.

scholarly journals Hippocampal Theta Oscillations Support Successful Associative Memory Formation

2020 ◽  
Vol 40 (49) ◽  
pp. 9507-9518 ◽  
Author(s):  
Srinivas Kota ◽  
Michael D. Rugg ◽  
Bradley C. Lega
Keyword(s):  
Associative Memory ◽  
Memory Formation ◽  
Theta Oscillations ◽  
Hippocampal Theta

The role of anterior and medial dorsal thalamus in associative memory encoding and retrieval

2020 ◽  
Vol 148 ◽  
pp. 107623 ◽  
Author(s):  
Kirk T. Geier ◽  
Bradley R. Buchsbaum ◽  
Shireen Parimoo ◽  
Rosanna K. Olsen
Keyword(s):  
Associative Memory ◽  
Memory Encoding ◽  
Dorsal Thalamus ◽  
Medial Dorsal ◽  
Encoding And Retrieval

scholarly journals The Sync/deSync model: How a synchronized hippocampus and a de-synchronized neocortex code memories

2017 ◽  
Author(s):  
George Parish ◽  
Simon Hanslmayr ◽  
Howard Bowman
Keyword(s):  
Neural Network ◽  
Network Model ◽  
Neural Network Model ◽  
Memory Formation ◽  
Spiking Neural Network ◽  
Memory Encoding ◽  
Oscillatory Dynamics ◽  
Theta Phase ◽  
Hippocampal Theta

AbstractNeural oscillations are important for memory formation in the brain. The de-synchronisation of Alpha (10Hz) oscillations in the neo-cortex has been shown to predict successful memory encoding and retrieval. However, when engaging in learning, it has been found that the hippocampus synchronises in Theta (4Hz) oscillations, and that learning is dependent on the phase of Theta. This inconsistency as to whether synchronisation is ‘good’ for memory formation leads to confusion over which oscillations we should expect to see and where during learning paradigm experiments. This paper seeks to respond to this inconsistency by presenting a neural network model of how a well-functioning learning system could exhibit both of these phenomena, i.e. desynchronization of alpha and synchronisation of theta during successful memory encoding.We present a spiking neural network (the Sync/deSync model) of the neo-cortical and hippocampal system. The simulated hippocampus learns through an adapted spike-time dependent plasticity rule, in which weight change is modulated by the phase of an extrinsically generated theta oscillation. Additionally, a global passive weight decay is incorporated, which is also modulated by theta phase. In this way, the Sync/deSync model exhibits theta phase-dependent long-term potentiation and long-term depression. We simulated a learning paradigm experiment and compared the oscillatory dynamics of our model with those observed in single-cell and scalp-EEG studies of the medial temporal lobe. Our Sync/deSync model suggests that both the de-synchronisation of neo-cortical Alpha and the synchronisation of hippocampal Theta are necessary for successful memory encoding and retrieval.Significance statementA fundamental question is the role of rhythmic activation of neurons, i.e. how their firing oscillates between high and low rates. A particularly important question is how oscillatory dynamics between the neo-cortex and hippocampus contribute to memory formation. We present a spiking neural-network model of such memory formation, with the central ideas that 1) in neo-cortex, neurons need to break-out of an alpha oscillation in order to represent a stimulus (i.e. alpha desynchronises), while 2) in hippocampus, the firing of neurons at theta facilitates formation of memories (i.e. theta synchronises). Accordingly, successful memory formation is marked by reduced neo-cortical alpha and increased hippocampal theta. This pattern has been observed experimentally and gives our model its name – the Synch/deSynch model.

scholarly journals Encoding and retrieval of associative recognition memory engage different sub-networks within a hippocampal-thalamo-cortical memory circuit

2021 ◽  
Author(s):  
Gareth Barker ◽  
Stephanie Tran ◽  
Kerry Gilroy ◽  
Zafar Bashir ◽  
Elizabeth Warburton
Keyword(s):  
Recognition Memory ◽  
Neural Activity ◽  
Associative Recognition ◽  
Memory Encoding ◽  
Nucleus Reuniens ◽  
Memory Circuit ◽  
Related Information ◽  
Ca1 Region ◽  
Key Nodes ◽  
Encoding And Retrieval

Abstract Recognition of previously encountered stimuli and their associated spatial and temporal information depends on neural activity within a brain-wide network in which the CA1 region of the hippocampus, nucleus reuniens of the thalamus (NRe) and medial prefrontal cortex (mPFC) are key nodes. However, the pathways crucial for coordinating activity during memory encoding and/or retrieval phases have been little explored. Here we opto- or chemo associative recognition memory. We discovered that encoding, but not retrieval depended on the CA1 to mPFC and NRe to mPFC projections. In contrast, retrieval depended on the mPFC to NRe projection. Interestingly the NRe to CA1 pathway was required for both memory phases. Our findings therefore reveal that encoding and retrieval engage dissociable sub-networks within a hippocampal-thalamo-cortical recognition memory circuit in order to enable binding of recent and related information, whilst ensuring a separation of processing.

scholarly journals Functional Interactions between Entorhinal Cortical Pathways Modulate Theta Activity in the Hippocampus

Biology ◽  
2021 ◽  
Vol 10 (8) ◽  
pp. 692
Author(s):  
Víctor J. López-Madrona ◽  
Santiago Canals
Keyword(s):  
Memory Formation ◽  
Theta Activity ◽  
Neuronal Firing ◽  
Theta Oscillations ◽  
Behavioral State ◽  
Phase Coupling ◽  
Hippocampal Theta Activity ◽  
Functional Interactions ◽  
Hippocampal Theta ◽  
Analytical Tools

Theta oscillations organize neuronal firing in the hippocampus during context exploration and memory formation. Recently, we have shown that multiple theta rhythms coexist in the hippocampus, reflecting the activity in their afferent regions in CA3 (Schaffer collaterals) and the entorhinal cortex layers II (EC-II, perforant pathway) and III (EC-III, temporoammonic pathway). Frequency and phase coupling between theta rhythms were modulated by the behavioral state, with synchronized theta rhythmicity preferentially occurring in tasks involving memory updating. However, information transmission between theta generators was not investigated. Here, we used source separation techniques to disentangle the current generators recorded in the hippocampus of rats exploring a known environment with or without a novel stimulus. We applied analytical tools based on Granger causality and transfer entropy to investigate linear and non-linear directed interactions, respectively, between the theta activities. Exploration in the novelty condition was associated with increased theta power in the generators with EC origin. We found a significant directed interaction from the Schaffer input over the EC-III input in CA1, and a bidirectional interaction between the inputs in the hippocampus originating in the EC, likely reflecting the connection between layers II and III. During novelty exploration, the influence of the EC-II over the EC-III generator increased, while the Schaffer influence decreased. These results associate the increase in hippocampal theta activity and synchrony during novelty exploration with an increase in the directed functional connectivity from EC-II to EC-III.

scholarly journals Signal Complexity of Human Intracranial EEG Tracks Successful Associative-Memory Formation across Individuals

2018 ◽  
Vol 38 (7) ◽  
pp. 1744-1755 ◽  
Author(s):  
Timothy C. Sheehan ◽  
Vishnu Sreekumar ◽  
Sara K. Inati ◽  
Kareem A. Zaghloul
Keyword(s):  
Associative Memory ◽  
Memory Formation ◽  
Intracranial Eeg ◽  
Signal Complexity

scholarly journals Single-trial Phase Entrainment of Theta Oscillations in Sensory Regions Predicts Human Associative Memory Performance

2018 ◽  
Author(s):  
Danying Wang ◽  
Andrew Clouter ◽  
Qiaoyu Chen ◽  
Kimron L. Shapiro ◽  
Simon Hanslmayr
Keyword(s):  
Episodic Memory ◽  
Auditory Cortex ◽  
Associative Memory ◽  
Memory Performance ◽  
Memory Formation ◽  
Theta Oscillations ◽  
Memory Representation ◽  
Relative Timing ◽  
Single Trial ◽  
Phase Offset

AbstractEpisodic memories are rich in sensory information and often contain integrated information from different sensory modalities. For instance, we can store memories of a recent concert with visual and auditory impressions being integrated in one episode. Theta oscillations have recently been implicated in playing a causal role synchronizing and effectively binding the different modalities together in memory. However, an open question is whether momentary fluctuations in theta synchronization predict the likelihood of associative memory formation for multisensory events. To address this question we presented movies and sounds with their luminance and volume modulated at theta (4 Hz), with a phase offset at 0° or 180° with respect to each other. This allowed us to entrain the visual and auditory cortex in a synchronous (0°) or asynchronous manner (180°). Participants were asked to remember the association between a movie and a sound while having their EEG activity recorded. Associative memory performance was significantly enhanced in the synchronous (0°) compared to the asynchronous (180°) condition. Source-level analysis demonstrated that the physical stimuli effectively entrained their respective cortical areas with a corresponding phase offset. Importantly, the strength of entrainment during encoding correlated with the efficacy of associative memory such that small phase differences between visual and auditory cortex predicted a high likelihood of correct retrieval in a later recall test. These findings suggest that theta oscillations serve a specific function in the episodic memory system: Binding the contents of different modalities into coherent memory episodes.Significance StatementHow multi-sensory experiences are bound to form a coherent episodic memory representation is one of the fundamental questions in human episodic memory research. Evidence from animal literature suggests that the relative timing between an input and theta oscillations in the hippocampus is crucial for memory formation. We precisely controlled the timing between visual and auditory stimuli and the neural oscillations at 4 Hz using a multisensory entrainment paradigm. Human associative memory formation depends on coincident timing between sensory streams processed by the corresponding brain regions. We provide evidence for a significant role of relative timing of neural theta activity in human episodic memory on a single trial level, which reveals a crucial mechanism underlying human episodic memory.

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