Selective Coupling between Theta Phase and Neocortical Fast Gamma Oscillations during REM-Sleep in Mice

Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (<xref ref-type="bibr" rid="bib29">Sweeney-Reed et al., 2014</xref>). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

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Hippocampal-prefrontal theta coupling develops as mice become proficient in associative odorant discrimination learning

10.1101/2021.09.28.462143 ◽

2021 ◽

Author(s):

Daniel Ramirez-Gordillo ◽

Andrew A. Parra ◽

K. Ulrich Bayer ◽

Diego Restrepo

Keyword(s):

Learning And Memory ◽

Discrimination Learning ◽

Gamma Oscillations ◽

Oscillatory Activity ◽

Dependent Protein Kinase ◽

Dependent Protein ◽

Theta Phase ◽

Phase Amplitude ◽

The Brain

Learning and memory requires coordinated activity between different regions of the brain. Here we studied the interaction between medial prefrontal cortex (mPFC) and hippocampal dorsal CA1 during associative odorant discrimination learning in the mouse. We found that as the animal learns to discriminate odorants in a go-no go task the coupling of high frequency neural oscillations to the phase of theta oscillations (phase-amplitude coupling or PAC) changes in a manner that results in divergence between rewarded and unrewarded odorant-elicited changes in the theta-phase referenced power (tPRP) for beta and gamma oscillations. In addition, in the proficient animal there was a decrease in the coordinated oscillatory activity between CA1 and mPFC in the presence of the unrewarded odorant. Furthermore, the changes in PAC resulted in a marked increase in the accuracy for decoding odorant identity from tPRP when the animal became proficient. Finally, we studied the role of Ca2+/calmodulin-dependent protein kinase II α (CaMKIIα), a protein involved in learning and memory, in oscillatory neural processing in this task. We find that the accuracy for decoding the odorant identity from tPRP decreases in CaMKIIα knockout mice and that this accuracy correlates with behavioral performance. These results implicate a role for PAC and CaMKIIα in olfactory go-no go associative learning in the hippocampal-prefrontal circuit.

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Dynamic modulation of theta–gamma coupling during rapid eye movement sleep

SLEEP ◽

10.1093/sleep/zsz182 ◽

2019 ◽

Vol 42 (12) ◽

Cited By ~ 6

Author(s):

Mojtaba Bandarabadi ◽

Richard Boyce ◽

Carolina Gutierrez Herrera ◽

Claudio L Bassetti ◽

Sylvain Williams ◽

...

Keyword(s):

Eye Movement ◽

Rem Sleep ◽

Temporal Dynamics ◽

Brain Structures ◽

Rapid Eye Movement ◽

Sleep Episode ◽

Frequency Coupling ◽

Theta Phase ◽

Hippocampal Networks ◽

Cross Frequency Coupling

Abstract Theta phase modulates gamma amplitude in hippocampal networks during spatial navigation and rapid eye movement (REM) sleep. This cross-frequency coupling has been linked to working memory and spatial memory consolidation; however, its spatial and temporal dynamics remains unclear. Here, we first investigate the dynamics of theta–gamma interactions using multiple frequency and temporal scales in simultaneous recordings from hippocampal CA3, CA1, subiculum, and parietal cortex in freely moving mice. We found that theta phase dynamically modulates distinct gamma bands during REM sleep. Interestingly, we further show that theta–gamma coupling switches between recorded brain structures during REM sleep and progressively increases over a single REM sleep episode. Finally, we show that optogenetic silencing of septohippocampal GABAergic projections significantly impedes both theta–gamma coupling and theta phase coherence. Collectively, our study shows that phase-space (i.e. cross-frequency coupling) coding of information during REM sleep is orchestrated across time and space consistent with region-specific processing of information during REM sleep including learning and memory.

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GABA-Glutamate supramammillary neurons control theta and gamma oscillations in the dentate gyrus during paradoxical (REM) sleep

10.1101/584862 ◽

2019 ◽

Cited By ~ 1

Author(s):

Francesca Billwiller ◽

Laura Castillo ◽

Heba Elseedy ◽

Anton Ivanovich Ivanov ◽

Jennyfer Scapula ◽

...

Keyword(s):

Dentate Gyrus ◽

Rem Sleep ◽

Slow Wave Sleep ◽

Granule Cells ◽

Structural Connectivity ◽

Gamma Oscillations ◽

Network Activity ◽

Projection Neurons ◽

Theta Power ◽

Gamma Power

AbstractSeveral studies suggest that neurons from the lateral region of the SuM (SuML) innervating the dorsal dentate gyrus (DG) display a dual GABAergic and glutamatergic transmission and are specifically activated during paradoxical (REM) sleep (PS). The objective of the present study is to fully characterize the anatomical, neurochemical and electrophysiological properties of the SuML-DG projection neurons and to determine how they control DG oscillations and neuronal activation during PS and other vigilance states. For this purpose, we combine structural connectivity techniques using neurotropic viral vectors (rabies virus, AAV), neurochemical anatomy (immunohistochemistry, in situ hybridization) and imaging (light, electron and confocal microscopy) with in vitro (patch clamp) and in vivo (LFP, EEG) optogenetic and electrophysiological recordings performed in transgenic VGLUT2-cre male mice. At the cellular level, we show that the SuML-DG neurons co-release GABA and glutamate on dentate granule cells and increase the activity of a subset of DG granule cells. At the network level, we show that activation of the SuML-DG pathway increases theta power and frequency during PS as well as gamma power during PS and waking in the DG. At the behavioral level, we show that the activation of this pathway does not change animal behavior during PS, induces awakening during slow wave sleep and increases motor activity during waking. These results suggest that the SuML-DG pathway is capable of supporting the increase of theta and gamma power in the DG observed during PS and plays an important modulatory role of DG network activity during this state.Significant statementAn increase of theta and gamma power in the dentate gyrus (DG) is an hallmark of paradoxical (REM) sleep (PS) and is suggested to promote learning and memory consolidation by synchronizing hippocampal networks and increasing its outputs to cortical targets. However the neuronal networks involved in such control of DG activity during PS are poorly understood. The present study identifies a population of GABA/Glutamate neurons in the lateral supramammllary nucleus (SuML) innervating the DG that could support such control during PS. Indeed, we show that activation of these SuML-DG projections increase theta power and frequency as well as gamma power in the DG specifically during PS and modulate activity of a subset of DG granule cells.

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Ramelteon modulates gamma oscillations in the rat primary motor cortex during non-REM sleep

Journal of Pharmacological Sciences ◽

10.1016/j.jphs.2020.11.006 ◽

2021 ◽

Vol 145 (1) ◽

pp. 97-104

Author(s):

Airi Yoshimoto ◽

Kotaro Yamashiro ◽

Takeshi Suzuki ◽

Yuji Ikegaya ◽

Nobuyoshi Matsumoto

Keyword(s):

Motor Cortex ◽

Rem Sleep ◽

Primary Motor Cortex ◽

Gamma Oscillations

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Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

10.1101/758813 ◽

2019 ◽

Author(s):

Justin Losacco ◽

Daniel Ramirez-Gordillo ◽

Jesse Gilmer ◽

Diego Restrepo

Keyword(s):

Olfactory Bulb ◽

Field Potential ◽

Gamma Oscillations ◽

Brain Regions ◽

Spike Timing ◽

Potential Oscillations ◽

Theta Oscillation ◽

Beta Power ◽

Early Processing ◽

Theta Phase

AbstractLocal field potential oscillations reflect temporally coordinated neuronal ensembles— coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.SignificanceEarly processing of olfactory information takes place in circuits undergoing slow frequency theta oscillations generated by the interplay of olfactory input modulated by sniffing and centrifugal feedback from downstream brain areas. Studies in the hippocampus and cortex suggest that different information “chunks” are conveyed at different phases of the theta oscillation. Here we show that in the olfactory bulb, the first processing station in the olfactory system, the amplitude of high frequency gamma oscillations encodes for information on whether an odorant is rewarded when it is observed at the peak phase of the theta oscillation. Furthermore, encoding of information by the theta phase-referenced gamma oscillations becomes more accurate as the animal learns to differentiate two odorants.

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Theta and gamma oscillations in the rat hippocampus during attentive lever pressing

10.1101/243527 ◽

2018 ◽

Author(s):

A Lipponen ◽

H Tanila ◽

K Gurevicius

Keyword(s):

Gamma Oscillations ◽

Water Port ◽

Lever Pressing ◽

Gamma Rhythms ◽

Frequency Coupling ◽

Theta Phase ◽

Hippocampal Theta ◽

Dentate Hilus ◽

Cross Frequency Coupling

AbstractThe hippocampus is known to be pivotal for spatial memory but emerging evidence suggests its contribution to temporal memories as well. However, it is not clear how the hippocampus represents time and how it synchronizes spatial and temporal presentations into a coherent memory. We assessed the specific role of hippocampal theta and gamma oscillations and their interaction in short-term timing of motor reactions. Rats were trained to maintain lever pressing for 2.5 s and then to quickly release the lever and retrieve water reward from a nearby water port guided by a cue light. In essence, this task allows observation of hippocampal rhythms during timed anticipation when no overt movements take place. Then we implanted wire electrodes to five hippocampal layers for recording local field potentials during the task. Consistent with earlier reports, theta showed a declining trend during the lever press. We also found that fast-gamma declined in tandem with theta while slow-gamma showed an opposite trend. Theta-phase to gamma-amplitude cross-frequency coupling measured with modulation index (MI) varied significantly between the three task phases. Interestingly, also changes in MI were opposite for fast- and slow-gamma. The MI was also related to the task performance, so that during omission trials the MI for fast-gamma in CA1 was smaller than during trials with premature lever release. In addition, the MI in dentate hilus was higher during all error trials than during correctly performed trials. Collectively, these data suggest an important role of synchronization of hippocampal theta and gamma rhythms to timing of cued motor reactions.

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GABA–glutamate supramammillary neurons control theta and gamma oscillations in the dentate gyrus during paradoxical (REM) sleep

Brain Structure and Function ◽

10.1007/s00429-020-02146-y ◽

2020 ◽

Vol 225 (9) ◽

pp. 2643-2668 ◽

Cited By ~ 1

Author(s):

Francesca Billwiller ◽

Laura Castillo ◽

Heba Elseedy ◽

Anton Ivanovich Ivanov ◽

Jennyfer Scapula ◽

...

Keyword(s):

Dentate Gyrus ◽

Rem Sleep ◽

Slow Wave Sleep ◽

Granule Cells ◽

Structural Connectivity ◽

Gamma Oscillations ◽

Network Activity ◽

Projection Neurons ◽

Gamma Power

AbstractSeveral studies suggest that neurons from the lateral region of the SuM (SuML) innervating the dorsal dentate gyrus (DG) display a dual GABAergic and glutamatergic transmission and are specifically activated during paradoxical (REM) sleep (PS). The objective of the present study is to characterize the anatomical, neurochemical and electrophysiological properties of the SuML-DG projection neurons and to determine how they control DG oscillations and neuronal activation during PS and other vigilance states. For this purpose, we combine structural connectivity techniques using neurotropic viral vectors (rabies virus, AAV), neurochemical anatomy (immunohistochemistry, in situ hybridization) and imaging (light, electron and confocal microscopy) with in vitro (patch clamp) and in vivo (LFP, EEG) optogenetic and electrophysiological recordings performed in transgenic VGLUT2-cre male mice. At the cellular level, we show that the SuML-DG neurons co-release GABA and glutamate on dentate granule cells and increase the activity of a subset of DG granule cells. At the network level, we show that activation of the SuML-DG pathway increases theta power and frequency during PS as well as gamma power during PS and waking in the DG. At the behavioral level, we show that the activation of this pathway does not change animal behavior during PS, induces awakening during slow wave sleep and increases motor activity during waking. These results suggest that the SuML-DG pathway is capable of supporting the increase of theta and gamma power in the DG observed during PS and plays an important modulatory role of DG network activity during this state.

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Organization and engagement of a prefrontal-olfactory network during olfactory selective attention

10.1101/2021.09.04.458996 ◽

2021 ◽

Author(s):

Hillary L Cansler ◽

Estelle E in 't Zandt ◽

Kaitlin S. Carlson ◽

Waseh T Khan ◽

Minghong Ma ◽

...

Keyword(s):

Selective Attention ◽

Gamma Oscillations ◽

Brain Regions ◽

Field Potentials ◽

Active Sampling ◽

Attention Task ◽

Gamma Power ◽

Theta Phase ◽

To Receive ◽

The Brain

Sensory perception is profoundly shaped by attention. Attending to an odor strongly regulates if and how a smell is perceived – yet the brain systems involved in this process are unknown. Here we report integration of the medial prefrontal cortex (mPFC), a collection of brain regions integral to attention, with the olfactory system in the context of selective attention to odors. First, we used tracing methods to establish the tubular striatum (TuS, also known as the olfactory tubercle) as the primary olfactory region to receive direct mPFC input in rats. Next, we recorded local field potentials from the olfactory bulb (OB), mPFC, and TuS while rats completed an olfactory selective attention task. Gamma power and coupling of gamma oscillations with theta phase were consistently high as rats flexibly switched their attention to odors. Beta and theta synchrony between mPFC and olfactory regions were elevated as rats switched their attention to odors. Finally, we found that sniffing was consistent despite shifting attentional demands, suggesting that the mPFC-OB theta coherence is independent of changes in active sampling. Together, these findings begin to define an olfactory attention network wherein mPFC activity, as well as that within olfactory regions, are coordinated in manners based upon attentional states.

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Theta phase mediates deliberate action switching in human Supplementary Motor Areas

10.1101/2021.05.06.442965 ◽

2021 ◽

Author(s):

Giovanni Maffei ◽

Riccardo Zucca ◽

Jordi Ysard Puigbo ◽

Diogo Santos Pata ◽

Marco Galli ◽

...

Keyword(s):

Motor Task ◽

Gamma Oscillations ◽

Theta Oscillations ◽

Motor Sequence ◽

Action Execution ◽

Oscillatory Dynamics ◽

Theta Waves ◽

Phase Alignment ◽

Theta Phase ◽

Motor Areas

The ability to deliberately overwrite ongoing automatic actions is a necessary feature of adaptive behavior. It has been proposed that the supplementary motor areas (SMAs) operate as a controller that orchestrates the switching between automatic and deliberate processes by inhibiting ongoing behaviors and so facilitating the execution of alternative ones. In addition, previous studies support the involvement of SMAs theta waves (4-9 Hz) in cognitive control. However, the exact role of such oscillatory dynamics and their contribution to the control of action are not fully understood. To investigate the mechanisms by which the SMAs support direct control of deliberate behavior, we recorded intracranial electroencephalography (iEEG) activity in humans performing a motor sequence task. Subjects had to perform a "change of plans" motor task requiring habitual movements to be overwritten at unpredictable moments. We found that SMAs were exclusively active during trials that demand action reprogramming in response to the unexpected cue but were silent during automatic action execution. Importantly, SMAs activity was characterized by a distinct temporal pattern, expressed in a stereotypical phase alignment of theta oscillations. More specifically, single trial motor performance was correlated with the trial contribution to the global inter-trial phase coherence, with higher coherence associated with faster trials. In addition, theta phase modulated the amplitude of gamma oscillations, with higher cross-frequency coupling in faster trials. Our results suggest that within frontal cortical networks, theta oscillations could encode a control signal that promotes the execution of deliberate actions.

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