scholarly journals Cooling of medial septum reveals theta phase lag coordination of hippocampal cell assemblies

2019 ◽  
Author(s):  
Peter C. Petersen ◽  
György Buzsáki
Keyword(s):  
Spatial Navigation ◽  
Medial Septum ◽  
Neuronal Firing ◽  
Theta Oscillations ◽  
Phase Lag ◽  
Cell Assemblies ◽  
Theta Frequency ◽  
Theta Phase ◽  
Temperature Manipulation ◽  
Phase Coordination

SummaryHippocampal theta oscillations coordinate neuronal firing to support memory and spatial navigation. The medial septum (MS) is critical in theta generation by two possible mechanisms: either a unitary ‘pacemaker’ timing signal is imposed on the hippocampal system or it may assist in organizing target subcircuits within the phase space of theta oscillations. We used temperature manipulation of the MS to test these models. Cooling of the MS reduced both theta frequency and power, was associated with enhanced incidence of errors in a spatial navigation task but did not affect spatial correlates of neurons. MS cooling decreased theta frequency oscillations of place cells, reduced distance-time compression but preserved distance-phase compression of place field sequences within the theta cycle. Thus, septal computation contributes not only theta pacing but is also critical for sustaining precise theta phase-coordination of cell assemblies in the hippocampus.

scholarly journals Cooling of Medial Septum Reveals Theta Phase Lag Coordination of Hippocampal Cell Assemblies

Neuron ◽  
2020 ◽  
Vol 107 (4) ◽  
pp. 731-744.e3 ◽  
Author(s):  
Peter Christian Petersen ◽  
György Buzsáki
Keyword(s):  
Medial Septum ◽  
Phase Lag ◽  
Cell Assemblies ◽  
Hippocampal Cell ◽  
Theta Phase

scholarly journals Shared rhythmic subcortical GABAergic input to the entorhinal cortex and presubiculum

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Tim James Viney ◽  
Minas Salib ◽  
Abhilasha Joshi ◽  
Gunes Unal ◽  
Naomi Berry ◽  
...  
Keyword(s):  
Entorhinal Cortex ◽  
Gamma Oscillations ◽  
Medial Septum ◽  
Theta Oscillations ◽  
Cortical Circuits ◽  
Cellular Mechanisms ◽  
Neuronal Synchrony ◽  
Theta Frequency ◽  
Episodic Memories ◽  
Gabaergic Modulation

Rhythmic theta frequency (~5–12 Hz) oscillations coordinate neuronal synchrony and higher frequency oscillations across the cortex. Spatial navigation and context-dependent episodic memories are represented in several interconnected regions including the hippocampal and entorhinal cortices, but the cellular mechanisms for their dynamic coupling remain to be defined. Using monosynaptically-restricted retrograde viral tracing in mice, we identified a subcortical GABAergic input from the medial septum that terminated in the entorhinal cortex, with collaterals innervating the dorsal presubiculum. Extracellularly recording and labeling GABAergic entorhinal-projecting neurons in awake behaving mice show that these subcortical neurons, named orchid cells, fire in long rhythmic bursts during immobility and locomotion. Orchid cells discharge near the peak of hippocampal and entorhinal theta oscillations, couple to entorhinal gamma oscillations, and target subpopulations of extra-hippocampal GABAergic interneurons. Thus, orchid cells are a specialized source of rhythmic subcortical GABAergic modulation of ‘upstream’ and ‘downstream’ cortico-cortical circuits involved in mnemonic functions.

scholarly journals The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats

2015 ◽  
Vol 113 (6) ◽  
pp. 1831-1841 ◽  
Author(s):  
San-San A. Chee ◽  
Janet L. Menard ◽  
Hans C. Dringenberg
Keyword(s):  
Medial Septum ◽  
Theta Activity ◽  
Lateral Septum ◽  
Theta Oscillations ◽  
Gating Mechanism ◽  
Plus Maze ◽  
Theta Frequency ◽  
Hippocampal Theta ◽  
Precise Role

Hippocampal theta oscillations are linked to various processes, including locomotion, learning and memory, and defense and affect. The lateral septum (LS) has been implicated in the generation of the hippocampal theta rhythm, but its precise role in this process is not well understood. Here, we investigated the effects of direct pharmacological inhibition or disinhibition of the dorsal LS (dLS) on the frequency of hippocampal theta activity elicited by stimulation of the reticular formation in urethane-anesthetized rats. We found that bilateral infusions of the GABAA receptor agonist muscimol into the dLS significantly increased theta frequency. Strikingly, intra-dLS infusions of the GABAA receptor antagonist GABAzine largely abolished reticularly elicited theta activity. We also locally injected these same compounds into the medial septum (MS) to test for neuroanatomical specificity. In contrast to the effects seen in the dLS, intra-MS infusions of muscimol had no effect on theta frequency, whereas intra-MS infusions of GABAzine increased theta frequency. Given the hypothesized role of hippocampal theta in behavioral defense, we also examined the effects of intra-dLS application of muscimol in two models of anxiety, the elevated plus maze and the novelty-induced suppression of feeding paradigm; both tests revealed clear, anxiolytic-like effects following muscimol infusions. The fact that dLS-muscimol increased theta frequency while also reducing anxiety-like behaviors challenges the influential theta suppression model of anxiolysis, which predicts a slowing of theta with anxiolytic compounds. More importantly, the experiments reveal a novel role of the LS, especially its dorsal aspects, as an important gating mechanism for the expression of theta oscillations in the rodent hippocampus.

scholarly journals Theta Phase Synchronization between the Human Hippocampus and Prefrontal Cortex Increases during Encoding of Unexpected Information: A Case Study

2018 ◽  
Vol 30 (11) ◽  
pp. 1646-1656 ◽  
Author(s):  
Matthias J. Gruber ◽  
Liang-Tien Hsieh ◽  
Bernhard P. Staresina ◽  
Christian E. Elger ◽  
Juergen Fell ◽  
...  
Keyword(s):  
Phase Synchronization ◽  
Theta Oscillations ◽  
Pharmacoresistant Epilepsy ◽  
Intracranial Eeg ◽  
Human Hippocampus ◽  
Electrophysiological Recordings ◽  
Theta Frequency ◽  
Rhinal Cortex ◽  
Theta Phase

Events that violate predictions are thought to not only modulate activity within the hippocampus and PFC but also enhance communication between the two regions. Scalp and intracranial EEG studies have shown that oscillations in the theta frequency band are enhanced during processing of contextually unexpected information. Some theories suggest that the hippocampus and PFC interact during processing of unexpected events, and it is possible that theta oscillations may mediate these interactions. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and PFC from two patients undergoing presurgical evaluation for pharmacoresistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal–prefrontal theta phase synchronization was significantly higher during encoding of contextually unexpected study items, relative to contextually expected study items. Furthermore, the hippocampal–prefrontal theta phase synchronization was larger for contextually unexpected items that were later remembered compared with later forgotten items. Moreover, we did not find increased theta synchronization between the PFC and rhinal cortex, suggesting that the observed effects were specific to prefrontal–hippocampal interactions. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and PFC in support of enhanced encoding of contextually deviant information.

scholarly journals Modulation of human intracranial theta oscillations during freely moving spatial navigation and memory

2019 ◽  
Author(s):  
Zahra M. Aghajan ◽  
Diane Villaroman ◽  
Sonja Hiller ◽  
Tyler J. Wishard ◽  
Uros Topalovic ◽  
...  
Keyword(s):  
Episodic Memory ◽  
Spatial Memory ◽  
High Frequency ◽  
Medial Temporal Lobe ◽  
Spatial Navigation ◽  
Grid Cell ◽  
Cell System ◽  
Theta Oscillations ◽  
Neural Basis ◽  
Freely Moving

SummaryHow the human brain supports accurate navigation of a learned environment has been an active topic of research for nearly a century1–5. In rodents, the theta rhythm within the medial temporal lobe (MTL) has been proposed as a neural basis for fragmenting incoming information and temporally organizing experiences and is thus widely implicated in spatial and episodic memory6. In addition, high-frequency theta (~8Hz) is associated with navigation, and loss of theta results in spatial memory deficits in rats 7. Recently, high-frequency theta oscillations during ambulatory movement have been identified in humans8,9, though their relationship to spatial memory remains unexplored. Here, we were able to record MTL activity during spatial memory and navigation in freely moving humans immersed in a room-scale virtual reality (VR) environment. Naturalistic movements were captured using motion tracking combined with wireless VR in participants implanted with an intracranial electroencephalographic (iEEG) recording system for the treatment of epilepsy. We found that prevalence of theta oscillations across brain sites during both learning and recall of spatial locations during ambulatory navigation is critically linked to memory performance. This finding supports the reinstatement hypothesis of episodic memory—thought to underlie our ability to recreate a prior experience10–12—and suggests that theta prevalence within the MTL may act as a potential representational state for memory reinstatement during spatial navigation. Additionally, we found that theta power is hexadirectionally modulated13–15 as a function of the direction of physical movement, most prominently after learning has occurred. This effect bears a resemblance to the rodent grid cell system16 and suggests an analog in human navigation. Taken together, our results provide the first characterization of neural oscillations in the human MTL during ambulatory spatial memory tasks and provide a platform for future investigations of neural mechanisms underlying freely moving navigation in humans.

scholarly journals Flexible theta sequence compression mediated via phase precessing interneurons

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Angus Chadwick ◽  
Mark CW van Rossum ◽  
Matthew F Nolan
Keyword(s):  
Action Potentials ◽  
High Capacity ◽  
Theta Oscillations ◽  
Sequence Generation ◽  
Spike Sequences ◽  
Theta Frequency ◽  
Neural Substrate ◽  
Hippocampal Theta ◽  
Novel Model ◽  
Sequence Compression

Encoding of behavioral episodes as spike sequences during hippocampal theta oscillations provides a neural substrate for computations on events extended across time and space. However, the mechanisms underlying the numerous and diverse experimentally observed properties of theta sequences remain poorly understood. Here we account for theta sequences using a novel model constrained by the septo-hippocampal circuitry. We show that when spontaneously active interneurons integrate spatial signals and theta frequency pacemaker inputs, they generate phase precessing action potentials that can coordinate theta sequences in place cell populations. We reveal novel constraints on sequence generation, predict cellular properties and neural dynamics that characterize sequence compression, identify circuit organization principles for high capacity sequential representation, and show that theta sequences can be used as substrates for association of conditioned stimuli with recent and upcoming events. Our results suggest mechanisms for flexible sequence compression that are suited to associative learning across an animal’s lifespan.

scholarly journals Optogenetic activation of SST-positive interneurons restores hippocampal theta oscillation impairment induced by soluble amyloid beta oligomersin vivo

2018 ◽  
Author(s):  
Hyowon Chung ◽  
Kyerl Park ◽  
Hyun Jae Jang ◽  
Michael M Kohl ◽  
Jeehyun Kwag
Keyword(s):  
Learning And Memory ◽  
Peak Power ◽  
Pyramidal Neurons ◽  
Hippocampal Slices ◽  
Field Potential ◽  
Theta Oscillations ◽  
Ca1 Pyramidal Neurons ◽  
Theta Frequency ◽  
Hippocampal Theta

AbstractAbnormal accumulation of amyloid β oligomers (AβO) is a hallmark of Alzheimer’s disease (AD), which leads to learning and memory deficits. Hippocampal theta oscillations that are critical in spatial navigation, learning and memory are impaired in AD. Since GABAergic interneurons, such as somatostatin-positive (SST+) and parvalbumin-positive (PV+) interneurons, are believed to play key roles in the hippocampal oscillogenesis, we asked whether AβO selectively impairs these SST+ and PV+ interneurons. To selectively manipulate SST+ or PV+ interneuron activity in mice with AβO pathologyin vivo, we co-injected AβO and adeno-associated virus (AAV) for expressing floxed channelrhodopsin-2 (ChR2) into the hippocampus of SST-Cre or PV-Cre mice. Local field potential (LFP) recordingsin vivoin these AβO–injected mice showed a reduction in the peak power of theta oscillations and desynchronization of spikes from CA1 pyramidal neurons relative to theta oscillations compared to those in control mice. Optogenetic-activation of SST+ but not PV+ interneurons in AβO–injected mice fully restored the peak power of theta oscillations and resynchronized the theta spike phases to a level observed in control mice.In vitrowhole-cell voltage-clamp recordings in CA1 pyramidal neurons in hippocampal slices treated with AβO revealed that short-term plasticity of SST+ interneuron inhibitory inputs to CA1 pyramidal neurons at theta frequency were selectively disrupted while that of PV+ interneuron inputs were unaffected. Together, our results suggest that dysfunction in inputs from SST+ interneurons to CA1 pyramidal neurons may underlie the impairment of theta oscillations observed in AβO-injected micein vivo.Our findings identify SST+ interneurons as a target for restoring theta-frequency oscillations in early AD.

scholarly journals Learning to synchronize: Midfrontal theta dynamics during rule switching

2020 ◽  
Author(s):  
Pieter Verbeke ◽  
Kate Ergo ◽  
Esther De Loof ◽  
Tom Verguts
Keyword(s):  
Negative Feedback ◽  
Human Subjects ◽  
Learning Task ◽  
Theta Oscillations ◽  
Prediction Errors ◽  
Hierarchical Learning ◽  
Theta Power ◽  
Negative Prediction ◽  
Theta Phase ◽  
The Brain

AbstractIn recent years, several hierarchical extensions of well-known learning algorithms have been proposed. For example, when stimulus-action mappings vary across time or context, the brain may learn two or more stimulus-action mappings in separate modules, and additionally (at a hierarchically higher level) learn to appropriately switch between those modules. However, how the brain mechanistically coordinates neural communication to implement such hierarchical learning, remains unknown. Therefore, the current study tests a recent computational model that proposed how midfrontal theta oscillations implement such hierarchical learning via the principle of binding by synchrony (Sync model). More specifically, the Sync model employs bursts at theta frequency to flexibly bind appropriate task modules by synchrony. 64-channel EEG signal was recorded while 27 human subjects (Female: 21, Male: 6) performed a probabilistic reversal learning task. In line with the Sync model, post-feedback theta power showed a linear relationship with negative prediction errors, but not with positive prediction errors. This relationship was especially pronounced for subjects with better behavioral fit (measured via AIC) of the Sync model. Also consistent with Sync model simulations, theta phase-coupling between midfrontal electrodes and temporo-parietal electrodes was stronger after negative feedback. Our data suggest that the brain uses theta power and synchronization for flexibly switching between task rule modules, as is useful for example when multiple stimulus-action mappings must be retained and used.Significance StatementEveryday life requires flexibility in switching between several rules. A key question in understanding this ability is how the brain mechanistically coordinates such switches. The current study tests a recent computational framework (Sync model) that proposed how midfrontal theta oscillations coordinate activity in hierarchically lower task-related areas. In line with predictions of this Sync model, midfrontal theta power was stronger when rule switches were most likely (strong negative prediction error), especially in subjects who obtained a better model fit. Additionally, also theta phase connectivity between midfrontal and task-related areas was increased after negative feedback. Thus, the data provided support for the hypothesis that the brain uses theta power and synchronization for flexibly switching between rules.

scholarly journals Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Catherine M Sweeney-Reed ◽  
Tino Zaehle ◽  
Jürgen Voges ◽  
Friedhelm C Schmitt ◽  
Lars Buentjen ◽  
...  
Keyword(s):  
Human Memory ◽  
Gamma Oscillations ◽  
Memory Formation ◽  
Anterior Thalamic Nucleus ◽  
Memory Processing ◽  
Phase Alignment ◽  
Theta Frequency ◽  
Frequency Coupling ◽  
Theta Phase ◽  
Cross Frequency Coupling

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.

scholarly journals Alternating sequences of future and past behavior encoded within hippocampal theta oscillations

Science ◽  
2020 ◽  
Vol 370 (6513) ◽  
pp. 247-250 ◽  
Author(s):  
Mengni Wang ◽  
David J. Foster ◽  
Brad E. Pfeiffer
Keyword(s):  
Activity Patterns ◽  
Place Cells ◽  
Theta Oscillations ◽  
Retrospective Evaluation ◽  
Past Behavior ◽  
Hippocampal Ca1 ◽  
Ongoing Behavior ◽  
Theta Phase ◽  
Hippocampal Theta ◽  
And Storage

Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.

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