Theta dominates cross-frequency coupling in hippocampal-medial entorhinal circuit during awake-behavior in rats

Zhou, Yuchen; Sheremet, A.; Kennedy, Jack P; Qin, Yu; DiCola, Nicholas M; Lovett, Sarah D.; Burke, Sara N.; Maurer, Andrew P.

doi:10.1016/j.isci.2022.105457

Cited by 9 publications

(8 citation statements)

References 121 publications

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“…In vivo , excitatory inputs from the entorhinal cortex to the dentate gyrus are most coherent in the theta band, while gamma oscillations would be generated locally from presumed local inhibitory inputs (Pernía-Andrade and Jonas, 2014 ). This predominance of theta over gamma coherence has also been reported between hippocampal CA1 and the medial entorhinal cortex (Zhou et al, 2022 ). Another potential pitfall in the communication-through-coherence hypothesis is that theta oscillations harmonics could overlap with higher frequency bands (Czurkó et al, 1999 ; Terrazas et al, 2005 ) including slow gamma (Petersen and Buzsáki, 2020 ).…”

Section: Gamma Oscillations Could Facilitate Communication Between Pr...supporting

confidence: 73%

Linking temporal coordination of hippocampal activity to memory function

Etter,

Carmichael,

Williams

2023

Front. Cell. Neurosci.

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Oscillations in neural activity are widespread throughout the brain and can be observed at the population level through the local field potential. These rhythmic patterns are associated with cycles of excitability and are thought to coordinate networks of neurons, in turn facilitating effective communication both within local circuits and across brain regions. In the hippocampus, theta rhythms (4–12 Hz) could contribute to several key physiological mechanisms including long-range synchrony, plasticity, and at the behavioral scale, support memory encoding and retrieval. While neurons in the hippocampus appear to be temporally coordinated by theta oscillations, they also tend to fire in sequences that are developmentally preconfigured. Although loss of theta rhythmicity impairs memory, these sequences of spatiotemporal representations persist in conditions of altered hippocampal oscillations. The focus of this review is to disentangle the relative contribution of hippocampal oscillations from single-neuron activity in learning and memory. We first review cellular, anatomical, and physiological mechanisms underlying the generation and maintenance of hippocampal rhythms and how they contribute to memory function. We propose candidate hypotheses for how septohippocampal oscillations could support memory function while not contributing directly to hippocampal sequences. In particular, we explore how theta rhythms could coordinate the integration of upstream signals in the hippocampus to form future decisions, the relevance of such integration to downstream regions, as well as setting the stage for behavioral timescale synaptic plasticity. Finally, we leverage stimulation-based treatment in Alzheimer's disease conditions as an opportunity to assess the sufficiency of hippocampal oscillations for memory function.

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Section: Gamma Oscillations Could Facilitate Communication Between Pr...supporting

confidence: 73%

Linking temporal coordination of hippocampal activity to memory function

Etter,

Carmichael,

Williams

2023

Front. Cell. Neurosci.

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“…As gamma is local, it should be considered that any “cross-regional correlation” in frequency has more to do with the common theta drive than frequency-specific communication ( Pernía-Andrade and Jonas, 2014 ; Ray and Maunsell, 2015 ). Gamma is the reverberatory consequence of common theta drive ( Mizuseki et al, 2009 ; Zhou et al, 2022 ). Future research should work toward understanding how the dynamic process of forming patterns within and propagating across regions supports higher cognitive functions.…”

Section: Discussionmentioning

confidence: 99%

Nonlinear Theta-Gamma Coupling between the Anterior Thalamus and Hippocampus Increases as a Function of Running Speed

Qin

Sheremet

Cooper

et al. 2023

eNeuro

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The hippocampal theta rhythm strongly correlates to awake behavior leading to theories that it represents a cognitive state of the brain. As theta has been observed in other regions of the Papez circuit, it has been theorized that activity propagates in a reentrant manner. These observations complement the energy cascade hypothesis in which large-amplitude, slow-frequency oscillations reflect activity propagating across a large population of neurons. Higher frequency oscillations, such as gamma, are related to the speed with which inhibitory and excitatory neurons interact and distribute activity on the local level. The energy cascade hypothesis suggests that the larger anatomical loops, maintaining theta, drive the smaller loops. As hippocampal theta increases in power with running speed, so does the power and frequency of the gamma rhythm. If theta is propagated through the circuit, it stands to reason that the local field potential recorded in other regions would be coupled to the hippocampal theta, with the coupling increasing with running speed. We explored this hypothesis using open-source simultaneous recorded data from the CA1 region of the hippocampus and the anterior dorsal and anterior ventral thalamus. Cross-regional theta coupling increased with running speed. Although the power of the gamma rhythm was lower in the anterior thalamus, there was an increase in the coupling of hippocampal theta to anterior thalamic gamma. Broadly, the data support models of how activity moves across the nervous system, suggesting that the brain uses large-scale volleys of activity to support higher cognitive processes.Significance StatementTheta and gamma are the local-field potential rhythms often studied in the hippocampal and entorhinal areas. However, these brain regions are only a component of the reentrant anatomy of the limbic system, suggesting that oscillatory interactions may reflect a more global process of neural organization. Here, we report theta and gamma interactions between hippocampus and the anterior dorsal and ventral nuclei of the thalamus that increase in strength as a function of running speed. These data reinforce the theory that larger rhythms are the physiological consequence of large-scale synaptic events across brain regions, where smaller oscillations represent the activity of a smaller synaptic pool.

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“…Recently, Zhou et al (2022) found there is little evidence of crossregional gamma-phase synchrony between MEC and HPC, suggesting local gamma oscillations are generated by interregional theta-inputs and local interneurons, rather than directly receiving interregional gamma-inputs (Zhou et al, 2022). The contribution of other interneuron cell-types for oscillatory generation is less known, while different types of interneurons fire at different timing of local oscillations (Klausberger & Somogyi, 2008;Valero & de la Prida, 2018).…”

Section: Cell-t Ype-s Pecifi C Oscill Atory Communi C Ati On In Mec-hp Cmentioning

confidence: 99%

“…These oscillatory activities are thought to be generated by inhibitory networks, especially PV + cells are considered to play key role and SOM + cells are important for gamma and ripple oscillations (Amilhon et al, 2015; Bartos et al, 2007; Bezaire et al, 2016; Buzsaki, 2015; Buzsaki & Wang, 2012; Korotkova et al, 2010; Royer et al, 2012; Schlingloff et al, 2014; Stark et al, 2014). Recently, Zhou et al (2022) found there is little evidence of cross‐regional gamma‐phase synchrony between MEC and HPC, suggesting local gamma oscillations are generated by interregional theta‐inputs and local interneurons, rather than directly receiving interregional gamma‐inputs (Zhou et al, 2022). The contribution of other interneuron cell‐types for oscillatory generation is less known, while different types of interneurons fire at different timing of local oscillations (Klausberger & Somogyi, 2008; Valero & de la Prida, 2018).…”

Section: Cell‐type‐specific Oscillatory Communication In Mec‐hpcmentioning

confidence: 99%

Dissecting cell‐type‐specific pathways in medial entorhinal cortical‐hippocampal network for episodic memory

Osanai

Nair

Kitamura

2023

Journal of Neurochemistry

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Episodic memory, which refers to our ability to encode and recall past events, is essential to our daily lives. Previous research has established that both the entorhinal cortex (EC) and hippocampus (HPC) play a crucial role in the formation and retrieval of episodic memories. However, to understand neural circuit mechanisms behind these processes, it has become necessary to monitor and manipulate the neural activity in a cell‐type‐specific manner with high temporal precision during memory formation, consolidation, and retrieval in the EC‐HPC networks. Recent studies using cell‐type‐specific labeling, monitoring, and manipulation have demonstrated that medial EC (MEC) contains multiple excitatory neurons that have differential molecular markers, physiological properties, and anatomical features. In this review, we will comprehensively examine the complementary roles of superficial layers of neurons (II and III) and the roles of deeper layers (V and VI) in episodic memory formation and recall based on these recent findings.

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Theta dominates cross-frequency coupling in hippocampal-medial entorhinal circuit during awake-behavior in rats

Cited by 9 publications

References 121 publications

Linking temporal coordination of hippocampal activity to memory function

Linking temporal coordination of hippocampal activity to memory function

Nonlinear Theta-Gamma Coupling between the Anterior Thalamus and Hippocampus Increases as a Function of Running Speed

Dissecting cell‐type‐specific pathways in medial entorhinal cortical‐hippocampal network for episodic memory

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