Phase-amplitude coupling and phase synchronization between medial temporal, frontal and posterior brain regions support episodic autobiographical memory recall

Episodic autobiographical memory (EAM) is a complex cognitive function that emerges from the coordination of specific and distant brain regions. Specific brain rhythms, namely theta and gamma oscillations and their synchronization, are thought of as putative mechanisms enabling EAM. Yet, the mechanisms of inter-regional interaction in the EAM network remain unclear in humans at the whole brain level. To investigate this, we analyzed EEG recordings of participants instructed to retrieve autobiographical episodes. EEG recordings were projected in the source space, and time-courses of atlas-based brain regions-of-interest (ROIs) were derived. Directed phase synchrony in high theta (7-10 Hz) and gamma (30-80 Hz) bands and high theta-gamma phase-amplitude coupling were computed between each pair of ROIs. Using network-based statistics, a graph-theory method, we found statistically significant networks for each investigated mechanism. In the gamma band, two sub-networks were found, one between the posterior cingulate cortex (PCC) and the medial temporal lobe (MTL) and another within the medial frontal areas. In the high theta band, we found a PCC to ventromedial prefrontal cortex (vmPFC) network. In phase-amplitude coupling, we found the high theta phase of the left MTL biasing the gamma amplitude of posterior regions and the vmPFC. Other regions of the temporal lobe and the insula were also phase biasing the vmPFC. These findings suggest that EAM, rather than emerging from a single mechanism at a single frequency, involves precise spatio-temporal signatures mapping on distinct memory processes. We propose that the MTL orchestrates activity in vmPFC and PCC via precise phase-amplitude coupling, with vmPFC and PCC interaction via high theta phase synchrony and gamma synchronization contributing to bind information within the PCC-MTL sub-network or valuate the candidate memory within the medial frontal sub-network.

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Spectral and Anatomical Patterns of Large-Scale Synchronization Predict Human Attentional Capacity

Cerebral Cortex ◽

10.1093/cercor/bhaa110 ◽

2020 ◽

Vol 30 (10) ◽

pp. 5293-5308 ◽

Cited By ~ 1

Author(s):

Santeri Rouhinen ◽

Felix Siebenhühner ◽

J Matias Palva ◽

Satu Palva

Keyword(s):

Visual Attention ◽

Large Scale ◽

Phase Synchronization ◽

Gamma Oscillations ◽

Brain Regions ◽

Functional Coupling ◽

Attentional Capacity ◽

Oscillation Phase ◽

Alpha Oscillation ◽

Phase Amplitude

Abstract The capacity of visual attention determines how many visual objects may be perceived at any moment. This capacity can be investigated with multiple object tracking (MOT) tasks, which have shown that it varies greatly between individuals. The neuronal mechanisms underlying capacity limits have remained poorly understood. Phase synchronization of cortical oscillations coordinates neuronal communication within the fronto-parietal attention network and between the visual regions during endogenous visual attention. We tested a hypothesis that attentional capacity is predicted by the strength of pretarget synchronization within attention-related cortical regions. We recorded cortical activity with magneto- and electroencephalography (M/EEG) while measuring attentional capacity with MOT tasks and identified large-scale synchronized networks from source-reconstructed M/EEG data. Individual attentional capacity was correlated with load-dependent strengthening of theta (3–8 Hz), alpha (8–10 Hz), and gamma-band (30–120 Hz) synchronization that connected the visual cortex with posterior parietal and prefrontal cortices. Individual memory capacity was also preceded by crossfrequency phase–phase and phase–amplitude coupling of alpha oscillation phase with beta and gamma oscillations. Our results show that good attentional capacity is preceded by efficient dynamic functional coupling and decoupling within brain regions and across frequencies, which may enable efficient communication and routing of information between sensory and attentional systems.

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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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Autobiographical Memory Retrieval and Hippocampal Activation as a Function of Repetition and the Passage of Time

Neural Plasticity ◽

10.1155/2007/90472 ◽

2007 ◽

Vol 2007 ◽

pp. 1-14 ◽

Cited By ~ 54

Author(s):

Lynn Nadel ◽

Jenna Campbell ◽

Lee Ryan

Keyword(s):

Autobiographical Memory ◽

Temporal Lobe ◽

Memory Retrieval ◽

Medial Temporal Lobe ◽

Perirhinal Cortex ◽

Brain Regions ◽

Long Term Memory ◽

Memory Traces ◽

Multiple Trace Theory

Multiple trace theory (MTT) predicts that hippocampal memory traces expand and strengthen as a function of repeated memory retrievals. We tested this hypothesis utilizing fMRI, comparing the effect of memory retrieval versus the mere passage of time on hippocampal activation. While undergoing fMRI scanning, participants retrieved remote autobiographical memories that had been previously retrieved either one month earlier, two days earlier, or multiple times during the preceding month. Behavioral analyses revealed that the number and consistency of memory details retrieved increased with multiple retrievals but not with the passage of time. While all three retrieval conditions activated a similar set of brain regions normally associated with autobiographical memory retrieval including medial temporal lobe structures, hippocampal activation did not change as a function of either multiple retrievals or the passage of time. However, activation in other brain regions, including the precuneus, lateral prefrontal cortex, parietal cortex, lateral temporal lobe, and perirhinal cortex increased after multiple retrievals, but was not influenced by the passage of time. These results have important implications for existing theories of long-term memory consolidation.

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

eLife ◽

10.7554/elife.52583 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 8

Author(s):

Justin Losacco ◽

Daniel Ramirez-Gordillo ◽

Jesse Gilmer ◽

Diego Restrepo

Keyword(s):

Olfactory Bulb ◽

Field Potential ◽

Brain Regions ◽

Spike Timing ◽

Potential Oscillations ◽

Neuronal Ensembles ◽

Beta Power ◽

High Gamma ◽

Theta Phase ◽

Phase Amplitude

Local 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.

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Odor induces characteristic time courses of theta, beta and gamma oscillations in human olfactory cortex

10.1101/2021.04.15.440045 ◽

2021 ◽

Author(s):

Qiaohan Yang ◽

Guangyu Zhou ◽

Gregory Lane ◽

Christina Zelano

Keyword(s):

Temporal Dynamics ◽

Piriform Cortex ◽

Gamma Oscillations ◽

Brain Regions ◽

Olfactory Cortex ◽

Odor Identification ◽

Temporal Properties ◽

Oscillatory Response ◽

Theta Phase ◽

Time Courses

Neuronal oscillations are fundamental to cognition, facilitating coordination and communication of information within and across brain regions. Studies on the spectral and temporal dynamics of oscillatory rhythms have contributed substantial insight to our understanding of mechanisms of human visual, auditory and somatosensory perception. However, these oscillations have been largely unexplored in the human olfactory system, where we lack basic understanding of fundamental spectrotemporal and functional properties. Determining if and how dynamic signatures of neural activity occur in human olfactory cortex is critical to understanding how we process odors. Here, we establish a characteristic oscillatory response to an odor in the human brain. Using direct electrical recordings from human piriform cortex, we identified three key odor-induced rhythms, in the theta (4-8Hz), beta (13-30Hz) and gamma (30-150Hz) frequency bands, each with distinct functional and temporal properties. While theta emerges and dissipates rapidly at the start of inhalation, beta and gamma emerge later, with beta persisting through exhalation, and gamma peaking around the transition between inhalation and exhalation. Beta and gamma amplitudes strongly predict odor identification ability, whereas theta does not. Theta phase modulates beta and gamma amplitudes during inhalation, only when odor is present. Our findings establish that smells elicit distinct neuronal rhythms in human olfactory cortex, which are dynamically interplayed over the course of a sniff. Our data further suggest a fundamental role for beta and gamma oscillations in human olfactory processing, and that their amplitudes--organized by theta phase--subserve odor identification in humans.

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Altered Temporal Structure of Neural Phase Synchrony in Patients With Autism Spectrum Disorder

Frontiers in Psychiatry ◽

10.3389/fpsyt.2021.618573 ◽

2021 ◽

Vol 12 ◽

Author(s):

Huibin Jia ◽

Fei Gao ◽

Dongchuan Yu

Keyword(s):

Autism Spectrum Disorder ◽

Time Series ◽

Temporal Structure ◽

Gamma Oscillations ◽

Brain Regions ◽

Autism Spectrum ◽

Spectrum Disorder ◽

Fluctuation Analysis ◽

Phase Synchrony ◽

Temporal Correlations

Functional connectivity, quantified by phase synchrony, between brain regions is known to be aberrant in patients with autism spectrum disorder (ASD). Here, we evaluated the long-range temporal correlations of time-varying phase synchrony (TV-PS) of electrocortical oscillations in patients with ASD as well as typically developing people using detrended fluctuation analysis (DFA) after validating the scale-invariance of the TV-PS time series. By comparing the DFA exponents between the two groups, we found that those of the TV-PS time series of high-gamma oscillations were significantly attenuated in patients with ASD. Furthermore, the regions involved in aberrant TV-PS time series were mainly within the social ability and cognition-related cortical networks. These results support the notion that abnormal social functions observed in patients with ASD may be caused by the highly volatile phase synchrony states of electrocortical oscillations.

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Anterior Nucleus of Thalamus Gates Progression of Mesial Temporal Seizures by Modulating Thalamocortical Synchrony

10.1101/2020.09.17.301812 ◽

2020 ◽

Author(s):

Ganne Chaitanya ◽

Adeel Ilyas ◽

Emilia Toth ◽

Diana Pizarro ◽

Kristen Riley ◽

...

Keyword(s):

Temporal Lobe ◽

Limbic System ◽

Phase Synchronization ◽

List Type ◽

Seizure Onset ◽

Anterior Nucleus ◽

Seizure Termination ◽

Temporal Lobe Seizures ◽

Temporal Lobe Seizure ◽

Phase Amplitude

AbstractThe anterior nucleus of the thalamus (ANT) mediates cortical-subcortical interactions between the limbic system and is hypothesized to facilitate the early organization of temporal lobe seizures. We set out to investigate the dynamic changes in synchronization parameters between the seizure onset zone (SOZ) and ANT during seizure stages (pre-onset to post-termination) in seven patients (n=26 seizures) with drug-resistant nonlesional temporal lobe epilepsy. Using local field potentials recorded directly from the limbic system and the ANT during stereoelectroencephalography, we confirm that the onset of mesial temporal lobe seizure is associated with increased thalamocortical network excitability and phase-amplitude coupling. The increase in thalamocortical phase synchronization preceded seizure onset, thereby suggesting that the early organization of temporal lobe seizures involves the integration of the ANT within the epileptic network. Towards seizure termination, there is a significant decrease in thalamic excitability, thalamocortical synchronization, and decoupling, thereby suggesting a breakdown in thalamocortical connectivity. A higher disease burden is significantly correlated with increased synchronization between the ANT and epileptic networks. Collectively, the results elucidate mechanistic insights and provide the temporal architecture of thalamocortical interactions that can be targeted in the rational designing of closed-loop seizure abortive interventions.HighlightsAnterior nucleus of thalamus is coactivated at the onset of temporal lobe seizuresIncrease thalamocortical synchronization and excitability is observed at seizure onsetSeizure termination is characterized by a breakdown in thalamocortical connectivityIncreased seizure burden affects thalamocortical synchronization

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Retrospective analysis of hemispheric structural network change as a function of location and size of glioma

Brain Communications ◽

10.1093/braincomms/fcaa216 ◽

2020 ◽

Author(s):

Shawn D’Souza ◽

Lisa Hirt ◽

David R Ormond ◽

John A Thompson

Keyword(s):

Diffusion Tensor Imaging ◽

White Matter ◽

Temporal Lobe ◽

Diffusion Tensor ◽

Brain Regions ◽

Structural Network ◽

Tumour Location ◽

The Impact ◽

Tractography Data ◽

Diffusion Tensor Imaging Tractography

Abstract Gliomas are neoplasms that arise from glial cell origin and represent the largest fraction of primary malignant brain tumours (77%). These highly infiltrative malignant cell clusters modify brain structure and function through expansion, invasion and intratumoral modification. Depending on the growth rate of the tumour, location and degree of expansion, functional reorganization may not lead to overt changes in behaviour despite significant cerebral adaptation. Studies in simulated lesion models and in patients with stroke reveal both local and distal functional disturbances, using measures of anatomical brain networks. Investigations over the last two decades have sought to use diffusion tensor imaging tractography data in the context of intracranial tumours to improve surgical planning, intraoperative functional localization, and post-operative interpretation of functional change. In this study, we used diffusion tensor imaging tractography to assess the impact of tumour location on the white matter structural network. To better understand how various lobe localized gliomas impact the topology underlying efficiency of information transfer between brain regions, we identified the major alterations in brain network connectivity patterns between the ipsilesional versus contralesional hemispheres in patients with gliomas localized to the frontal, parietal or temporal lobe. Results were indicative of altered network efficiency and the role of specific brain regions unique to different lobe localized gliomas. This work draws attention to connections and brain regions which have shared structural susceptibility in frontal, parietal and temporal lobe glioma cases. This study also provides a preliminary anatomical basis for understanding which affected white matter pathways may contribute to preoperative patient symptomology.

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