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

Griffiths, Benjamin; Parish, George; Roux, Frédéric; Michelmann, Sebastian; Plas, Mircea van der; Kolibius, Luca D.; Chelvarajah, Ramesh; Rollings, David T.; Sawlani, Vijay; Hamer, Hajo M.; Gollwitzer, Stephanie; Kreiselmeyer, Gernot; Staresina, Bernhard P.; Wimber, Maria; Hanslmayr, Simon

doi:10.1073/pnas.1914180116

Cited by 120 publications

(135 citation statements)

References 61 publications

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“…This effect may be determined because of direct connections (via entorhinal cortex) with regions supporting the formation of contextual memories, such as in the parahippocampal gyrus and the hippocampus (Bar et al, 2008;Davachi, 2006;Dundon et al, 2018). A recent study has demonstrated the interplay between semantic processing in ATL and information encoding/retrieval in the hippocampus during the formation/retrieval of contextual memories (Griffiths et al, 2019). Accordingly, it is possible that these anatomical connections allow these regions to cooperate for the formation and retrieval of semantic and contextual information conveyed in the narrative (e.g., episodic details) (Ranganath and Ritchey, 2012), facilitating the flow of neocortical information into the hippocampus during encoding and the propagation of hippocampal retrieval signals into the ATL during retrieval.…”

Section: Hubs For the Formation Of Time-extended Conceptual Gestaltmentioning

confidence: 99%

Revealing the neural networks that extract conceptual gestalts from continuously evolving or changing semantic contexts

Branzi

Humphreys

Hoffman

et al. 2019

Preprint

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AbstractReading a book, understanding the news reports or any other behaviour involving the processing of meaningful stimuli requires the semantic system to have two main features: being active during an extended period of time and flexibly adapting the internal representation according to the changing environment. Despite being key features of many everyday tasks, formation and updating of the semantic “gestalt” are still poorly understood. In this fMRI study we used naturalistic stimuli and task manipulations to identify the neural network that forms and updates conceptual gestalts during time-extended integration of meaningful stimuli. Univariate and multivariate techniques allowed at drawing a distinction between networks that are crucial for the formation of a semantic gestalt (meaning integration) and those that instead are important for linking incoming cues about the current context (e.g., time, space cues) into a schema representation. Specifically, we revealed that time-extended formation of the conceptual gestalt was reflected in the neurocomputations of the anterior temporal lobe accompanied by multi-demand areas and hippocampus, with a key role of brain structures in the right hemisphere. This “semantic gestalt network” was strongly recruited when an update of the current semantic representation was required during narrative processing. A distinct fronto-parietal network, instead, was recruited for context integration, independently from the meaning associations between words (semantic coherence). Finally, in contrast with accounts positing that the default-mode-network (DMN) may have a crucial role in semantic cognition, our findings revealed that DMN activity was sensitive to task difficulty, but not to semantic integration. The implications of these findings for neurocognitive models of semantic cognition and the literature on narrative processing are discussed.HighlightsfMRI revealed areas and networks for semantic integration during narrative readingATL has a key role in the formation of the conceptual gestaltIFG, pMTG and dAG reflect the update of the conceptual gestaltLeft AG (Mid-PGp) has a key role in context integration

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Section: Hubs For the Formation Of Time-extended Conceptual Gestaltmentioning

confidence: 99%

Revealing the neural networks that extract conceptual gestalts from continuously evolving or changing semantic contexts

Branzi

Humphreys

Hoffman

et al. 2019

Preprint

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“…Probing rat hippocampal neurons in vitro, Bi and Poo (1998) showed that the postsynaptic neuron must fire 20 ms (that is, 1 cycle of a gamma oscillation) after the presynaptic neuron to induce LTP. Given that these hippocampal neurons have been shown to lock gamma-band activity (Jutras, Fries, & Buffalo, 2009) and hippocampal gamma-band activity is predictive of memory formation (e.g., Griffiths et al, 2019;Long & Kahana, 2015), one could speculate that increases in the amplitude of hippocampal gamma oscillations reflect increases in STDP.…”

Section: A Role For Neural Oscillationsmentioning

confidence: 99%

Event conjunction: How the hippocampus integrates episodic memories across event boundaries

Griffiths

Fuentemilla

2019

Hippocampus

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Our lives are a continuous stream of experience. Our episodic memories on the other hand have a definitive beginning, middle, and end. Theories of event segmentation suggest that salient changes in our environment produce event boundaries which partition the past from the present and, as a result, produce discretized memories. However, event boundaries cannot completely discretize two memories; any shared conceptual link will lead to the rapid integration of these memories. Here, we present a new framework inspired by electrophysiological research that resolves this apparent contradiction. At its heart, the framework proposes that hippocampal theta‐gamma coupling maintains a highly abstract model of an ongoing event and serves to encode this model as an episodic memory. When a second but related event begins, this theta‐gamma model is rapidly reconstructed within the hippocampus where new details of the second event can be appended to the existing event model. The event conjunction framework is the first electrophysiological explanation of how event memories can be formed at, and integrated across, event boundaries.

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“…A memory-related increase in synchronisation can take the form of an increase in theta or gamma power (e.g. Burke et al, 2013;Griffiths, Parish, et al, 2019;Long & Kahana, 2015;Montgomery & Buzsáki, 2007;Osipova et al, 2006;Sederberg et al, 2007;Staresina et al, 2016), or an increase in the coupling between these two oscillations (e.g. Bahramisharif, Jensen, Jacobs, & Lisman, 2018;Heusser, Poeppel, Ezzyat, & Davachi, 2016;Staudigl & Hanslmayr, 2013;Tort, Komorowski, Manns, Kopell, & Eichenbaum, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…By coupling gamma power to the phase of theta that is optimal for LTP, the propensity for mnemonic binding is further enhanced. However, hippocampal activation during encoding is contingent on the amount of preceding neocortical desynchronisation, and vice versa during episodic memory retrieval (Griffiths, Parish, et al, 2019). Statistically speaking, it is therefore plausible to suggest that a single latent variable produces both neocortical desynchronisation and hippocampal synchronisation.…”

Section: Introductionmentioning

confidence: 99%

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

Griffiths

Martín-Buro

Staresina

et al. 2020

Preprint

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word count: 200 Introduction word count: 590 Discussion word count: 1,150Abstract Episodic memory relies on two processes: 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 neocortical alpha/beta desynchronisation while the second is thought to be supported by hippocampal theta and gamma synchronisation. However, recent empirical evidence suggests that these two neural phenomena are contingent on one another, questioning whether alpha/beta desynchronisation and theta/gamma synchronisation truly reflect distinct processes. Here, we addressed this conundrum by asking seventeen participants to complete a paradigm that temporally separated sensory information representation and mnemonic binding while undergoing MEG recordings. We found that, during the perception and retrieval of task-relevant information, neocortical alpha/beta power monotonically decreased with the number of items recalled from a sequence. During mnemonic binding however, hippocampal theta/gamma phase-amplitude coupling monotonically increased with the number of sequence items later recalled. These results suggest a double dissociation between neocortical alpha/beta and hippocampal theta/gamma activity, with alpha/beta desynchronisation uniquely relating to information representation and theta/gamma phase-amplitude coupling uniquely relating to mnemonic binding. As such, we conclude that alpha/beta desynchronisation and hippocampal theta/gamma synchronisation represent two separable processes in episodic memory. Significance StatementEpisodic memories are highly detailed snapshots of our personally experienced past. The formation and retrieval of episodic memories have consistently been shown to rely on the hippocampus and the sensory neocortex. However, it is unknown whether the memory-related neural activity in the hippocampus and neocortex reflect separate, interacting cognitive processes, or are two neural responses to a singular process.Here, we find evidence in favour of the former. Memory-related decreases in neocortical alpha/beta power uniquely arise to the perception and retrieval of event-related information, while memory-related increases in hippocampal theta/gamma phase-amplitude coupling uniquely arise during mnemonic binding. This double dissociation suggests that the neocortex and hippocampus play distinct and separable roles in the formation and retrieval of episodic memories

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

Cited by 120 publications

References 61 publications

Revealing the neural networks that extract conceptual gestalts from continuously evolving or changing semantic contexts

Revealing the neural networks that extract conceptual gestalts from continuously evolving or changing semantic contexts

Event conjunction: How the hippocampus integrates episodic memories across event boundaries

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

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