Ongoing Theta Rhythm Research Articles

Gamma oscillatory complexity conveys behavioral information in hippocampal networks

The hippocampus and entorhinal cortex exhibit rich oscillatory patterns critical for cognitive functions. In the hippocampal region CA1, specific gamma-frequency oscillations, timed at different phases of the ongoing theta rhythm, are hypothesized to facilitate the integration of information from varied sources and contribute to distinct cognitive processes. Here, we show that gamma elements -a multidimensional characterization of transient gamma oscillatory episodes- occur at any frequency or phase relative to the ongoing theta rhythm across all CA1 layers in male mice. Despite their low power and stochastic-like nature, individual gamma elements still carry behavior-related information and computational modeling suggests that they reflect neuronal firing. Our findings challenge the idea of rigid gamma sub-bands, showing that behavior shapes ensembles of irregular gamma elements that evolve with learning and depend on hippocampal layers. Widespread gamma diversity, beyond randomness, may thus reflect complexity, likely functional but invisible to classic average-based analyses.

Gamma amplitude is coupled to opposed hippocampal theta-phase states during the encoding and retrieval of episodic memories in humans

Computational models and invivo studies in rodents suggest that the emergence of gamma activity (40-140Hz) during memory encoding and retrieval is coupled to opposed-phase states of the underlying hippocampal theta rhythm (4-9Hz).1,2,3,4,5,6,7,8,9,10 However, direct evidence for whether human hippocampal gamma-modulated oscillatory activity in memory processes is coupled to opposed-phase states of the ongoing theta rhythm remains elusive. Here, we recorded local field potentials (LFPs) directly from the hippocampus of 10 patients with epilepsy, using depth electrodes. We used a memory encoding and retrieval task whereby trialunique sequences of pictures depicting real-life episodes were presented, and 24h later, participants were asked to recall them upon the appearance of the first picture of the encoded episodic sequence. Wefound theta-to-gamma cross-frequency coupling that was specific to the hippocampus during both the encoding and retrieval of episodic memories. We also revealed that gamma was coupled to opposing theta phases during both encoding and recall processes. Additionally, we observed that the degree of theta-gamma phase opposition between encoding and recall was associated with participants' memory performance, so gamma power was modulated by theta phase for both remembered and forgotten trials, although only for remembered trials the dominant theta phase was different for encoding and recall trials. The current results offer direct empirical evidence in support of hippocampal theta-gamma phase opposition models in human long-term memory and provide fundamental insights into mechanistic predictions derived from computational and animal work, thereby contributing to establishing similarities and differences across species.

Interictal Spike and Loss of Hippocampal Theta Rhythm Recorded by Deep Brain Electrodes during Epileptogenesis.

Epileptogenesis is the gradual dynamic process that progressively led to epilepsy, going through the latent stage to the chronic stage. During epileptogenesis, how the abnormal discharges make theta rhythm loss in the deep brain remains not clear. In this paper, a loss of theta rhythm was estimated based on time–frequency power using the longitudinal electroencephalography (EEG), recorded by deep brain electrodes (e.g., the intracortical microelectrodes such as stereo-EEG electrodes) with monitored epileptic spikes in a rat from the first region in the hippocampal circuit. Deep-brain EEG was collected from the period between adjacent sporadic interictal spikes (lasting 3.56 s—35.38 s) to the recovery period without spikes by videos while the rats were performing exploration. We found that loss of theta rhythm became more serious during the period between adjacent interictal spikes than during the recovery period without spike, and during epileptogenesis, more loss was observed at the acute stage than the chronic stage. We concluded that the emergence of the interictal spike was the direct cause of loss of theta rhythm, and the inhibitory effect of the interictal spike on ongoing theta rhythm was persistent as well as time dependent during epileptogenesis. With the help of the intracortical microelectrodes, this study provides a temporary proof of interictal spikes to produce ongoing theta rhythm loss, suggesting that the interictal spikes could correlate with the epileptogenesis process, display a time-dependent feature, and might be a potential biomarker to evaluate the deficits in theta-related memory in the brain.

Hippocampal Sequences During Exploration: Mechanisms and Functions.

Although the hippocampus plays a critical role in spatial and episodic memories, the mechanisms underlying memory formation, stabilization, and recall for adaptive behavior remain relatively unknown. During exploration, within single cycles of the ongoing theta rhythm that dominates hippocampal local field potentials, place cells form precisely ordered sequences of activity. These neural sequences result from the integration of both external inputs conveying sensory-motor information, and intrinsic network dynamics possibly related to memory processes. Their endogenous replay during subsequent sleep is critical for memory consolidation. The present review discusses possible mechanisms and functions of hippocampal theta sequences during exploration. We present several lines of evidence suggesting that these neural sequences play a key role in information processing and support the formation of initial memory traces, and discuss potential functional distinctions between neural sequences emerging during theta vs. awake sharp-wave ripples.

Theta-paced flickering between place-cell maps in the hippocampus: A model based on short-term synaptic plasticity.

Hippocampal place cells represent different environments with distinct neural activity patterns. Following an abrupt switch between two familiar configurations of visual cues defining two environments, the hippocampal neural activity pattern switches almost immediately to the corresponding representation. Surprisingly, during a transient period following the switch to the new environment, occasional fast transitions between the two activity patterns (flickering) were observed (Jezek, Henriksen, Treves, Moser, & Moser, 2011). Here we show that an attractor neural network model of place cells with connections endowed with short‐term synaptic plasticity can account for this phenomenon. A memory trace of the recent history of network activity is maintained in the state of the synapses, allowing the network to temporarily reactivate the representation of the previous environment in the absence of the corresponding sensory cues. The model predicts that the number of flickering events depends on the amplitude of the ongoing theta rhythm and the distance between the current position of the animal and its position at the time of cue switching. We test these predictions with new analysis of experimental data. These results suggest a potential role of short‐term synaptic plasticity in recruiting the activity of different cell assemblies and in shaping hippocampal activity of behaving animals.

Coordination of phase precession through feed-forward topologies in the hippocampus

The process of faithfully retrieving episodes from our memory requires a neural mechanism capable of initially forming ordered and reliable behavioral sequences. These behavioral sequences take place on a timescale of seconds or more whereas the timescale of neural plasticity and learning is in the order of tens of milliseconds. To shed light on this dilemma, we turn to studies of hippocampal place cells in rodents, i.e., cells that selectively increase their firing rates in locations of the environment known as the place fields. Within a field, the firing phases of a place cell precess monotonically relative to the ongoing theta rhythm. This phenomenon, termed “phase precession” [1], leads to a temporally compressed representation of the behavioral sequences experienced by the rodent [2], and the compressed timescale matches the requirements of neural plasticity. Phase precession has been observed in several regions of the hippocampus and entorhinal cortex, but it remains a mystery whether phase precession emerges independently in each region, or conversely, whether phase precession can be “inherited” from an upstream neuronal population. Here, we show how the simple feed-forward topologies in the hippocampal formation assist in propagating phase precession to different regions of the hippocampus and adjacent structures. We explain how the place-selective responses of a given cell are influenced by both excitation and inhibition and show that these responses are consistent with intracellular [3] and extracellular recordings in-vivo during phase precession [4][5]. Our results suggest that the presence of phase precession in different stages of the hippocampal circuit is indicative of a common source, a fact that can help us better understand sequence coding within the hippocampus.

The topographical N170: Electrophysiological evidence of a neural mechanism for human spatial navigation

We recently demonstrated that the latency of a component of the event-related brain potential, the topographical N170 (NT170), is sensitive to the spatial location of reward-related stimuli in a virtual maze environment, occurring earlier for rewards found following rightward turns compared to leftward turns. We suggested that this NT170 latency effect may result from phase reset of an ongoing theta rhythm by a parahippocampal system for spatial navigation. Here we tested several predictions that follow from this proposal, namely, that the effect is observed only when the rewards are presented in a spatial environment, that it is sensitive to individual differences in spatial ability, that it is localizable to the right parahippocampal region, and that it is consistent with partial phase resetting of an ongoing theta rhythm. These results hold promise for integrating ERP measures of spatial navigation with extensive animal, human, and computational literatures on parahippocampal function.

Locomotion-Related Oscillatory Body Movements at 6–12 Hz Modulate the Hippocampal Theta Rhythm

The hippocampal theta rhythm is required for accurate navigation and spatial memory but its relation to the dynamics of locomotion is poorly understood. We used miniature accelerometers to quantify with high temporal and spatial resolution the oscillatory movements associated with running in rats. Simultaneously, we recorded local field potentials in the CA1 area of the hippocampus. We report that when rats run their heads display prominent vertical oscillations with frequencies in the same range as the hippocampal theta rhythm (i.e., 6–12 Hz). In our behavioral set-up, rats run mainly with speeds between 50 and 100 cm/s. In this range of speeds, both the amplitude and frequency of the “theta” head oscillations were increasing functions of running speed, demonstrating that the head oscillations are part of the locomotion dynamics. We found evidence that these rhythmical locomotor dynamics interact with the neuronal activity in the hippocampus. The amplitude of the hippocampal theta rhythm depended on the relative phase shift with the head oscillations, being maximal when the two signals were in phase. Despite similarity in frequency, the head movements and LFP oscillations only displayed weak phase and frequency locking. Our results are consistent with that neurons in the CA1 region receive inputs that are phase locked to the head acceleration signal and that these inputs are integrated with the ongoing theta rhythm.

Hippocampal Theta-Phase Modulation of Replay Correlates with Configural-Relational Short-Term Memory Performance: Figure 1.

There is now growing evidence that the hippocampus generates theta rhythms that can phase bias fast neural oscillations in the neocortex, allowing coordination of widespread fast oscillatory populations outside limbic areas. A recent magnetoencephalographic study showed that maintenance of configural-relational scene information in a delayed match-to-sample (DMS) task was associated with replay of that information during the delay period. The periodicity of the replay was coordinated by the phase of the ongoing theta rhythm, and the degree of theta coordination during the delay period was positively correlated with DMS performance. Here, we reanalyzed these data to investigate which brain regions were involved in generating the theta oscillations that coordinated the periodic replay of configural-relational information. We used a beamformer algorithm to produce estimates of regional theta rhythms and constructed volumetric images of the phase-locking between the local theta cycle and the instances of replay (in the 13-80 Hz band). We found that individual differences in DMS performance for configural-relational associations were related to the degree of phase coupling of instances of cortical reactivations to theta oscillations generated in the right posterior hippocampus and the right inferior frontal gyrus. This demonstrates that the timing of memory reactivations in humans is biased toward hippocampal theta phase.

Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception.

Consciousness has been proposed to emerge from functionally integrated large-scale ensembles of gamma-synchronous neural populations that form and dissolve at a frequency in the theta band. We propose that discrete moments of perceptual experience are implemented by transient gamma-band synchronization of relevant cortical regions, and that disintegration and reintegration of these assemblies is time-locked to ongoing theta oscillations. In support of this hypothesis we provide evidence that (1) perceptual switching during binocular rivalry is time-locked to gamma-band synchronizations which recur at a theta rate, indicating that the onset of new conscious percepts coincides with the emergence of a new gamma-synchronous assembly that is locked to an ongoing theta rhythm; (2) localization of the generators of these gamma rhythms reveals recurrent prefrontal and parietal sources; (3) theta modulation of gamma-band synchronization is observed between and within the activated brain regions. These results suggest that ongoing theta-modulated-gamma mechanisms periodically reintegrate a large-scale prefrontal-parietal network critical for perceptual experience. Moreover, activation and network inclusion of inferior temporal cortex and motor cortex uniquely occurs on the cycle immediately preceding responses signaling perceptual switching. This suggests that the essential prefrontal-parietal oscillatory network is expanded to include additional cortical regions relevant to tasks and perceptions furnishing consciousness at that moment, in this case image processing and response initiation, and that these activations occur within a time frame consistent with the notion that conscious processes directly affect behaviour.

Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm

Theta phase-locking and phase precession are two related phenomena reflecting coordination of hippocampal place cell firing with the local, ongoing theta rhythm. The mechanisms and functions of both the phenomena remain unclear, though the robust correlation between firing phase and location of the animal has lead to the suggestion that this phase relationship constitutes a temporal code for spatial information. Recent work has described theta phase-locking in the rat medial prefrontal cortex (mPFC), a structure with direct anatomical and functional links to the hippocampus. Here, we describe an initial characterization of phase precession in the mPFC relative to the CA1 theta rhythm. mPFC phase precession was most robust during behavioral epochs known to be associated with enhanced theta-frequency coordination of CA1 and mPFC activities. Precession was coherent across the mPFC population, with multiple neurons precessing in parallel as a function of location of the animal. The existence of phase precession beyond the hippocampus implies a more global role for this phenomenon during theta rhythm-mediated coordination of neural activity.

A learning rule for place fields in a cortical model: Theta phase precession as a network effect

We show that a model of the hippocampus introduced recently by Scarpetta et al. (2002, Neural Computation 14(10):2371-2396) explains the theta phase precession phenomena. In our model, the theta phase precession comes out as a consequence of the associative-memory-like network dynamics, i.e., the network's ability to imprint and recall oscillatory patterns, coded both by phases and amplitudes of oscillation. The learning rule used to imprint the oscillatory states is a natural generalization of that used for static patterns in the Hopfield model, and is based on the spike-time-dependent synaptic plasticity, experimentally observed.In agreement with experimental findings, the place cells' activity appears at consistently earlier phases of subsequent cycles of the ongoing theta rhythm during a pass through the place field, while the oscillation amplitude of the place cells' firing rate increases as the animal approaches the center of the place field and decreases as the animal leaves the center. The total phase precession of the place cell is lower than 360 degrees , in agreement with experiments. As the animal enters a receptive field, the place cells' activity comes slightly less than 180 degrees after the phase of maximal pyramidal cell population activity, in agreement with the findings of Skaggs et al. (1996, Hippocampus 6:149-172). Our model predicts that the theta phase is much better correlated with location than with time spent in the receptive field. Finally, in agreement with the recent experimental findings of Zugaro et al. (2005, Nature Neuroscience 9(1):67-71), our model predicts that theta phase precession persists after transient intrahippocampal perturbation.

Theta reset produces optimal conditions for long-term potentiation.

Connections among theta rhythm, long-term potentiation (LTP) and memory in hippocampus are suggested by previous research, but definitive links are yet to be established. We investigated the hypothesis that resetting of local hippocampal theta to relevant stimuli in a working memory task produces optimal conditions for induction of LTP. The timings of the peak and trough of the first wave of reset theta were determined in initial sessions and used to time stimulation (4 pulses, 200 Hz) during subsequent performance. Stimulation on the peak of stimulus-reset theta produced LTP while stimulation on the trough did not. These results suggest that a memory-relevant stimulus produces a phase shift of ongoing theta rhythm that induces optimal conditions for the stimulus to undergo potentiation.

Information Transfer Between Rhythmically Coupled Networks: Reading the Hippocampal Phase Code

There are numerous reports on rhythmic coupling between separate brain networks. It has been proposed that this rhythmic coupling indicates exchange of information. So far, few computational models have been proposed that explore this principle and its potential computational benefits. Recent results on hippocampal place cells of the rat provide new insight; it has been shown that information about space is encoded by the firing of place cells with respect to the phase of the ongoing theta rhythm. This principle is termed phase coding and suggests that upcoming locations (predicted by the hippocampus) are encoded by cells firing late in the theta cycle, whereas current location is encoded by early firing in the theta cycle. A network reading the hippocampal output must inevitably also receive an oscillatory theta input in order to decipher the phase-coded firing patterns. In this article, I propose a simple physiologically plausible mechanism implemented as an oscillatory network that can decode the hippocampal output. By changing only the phase of the theta input to the decoder, qualitatively different information is transferred: the theta phase determines whether representations of current or upcoming locations are read by the decoder. The proposed mechanism provides a computational principle for information transfer between oscillatory networks and might generalize to brain networks beyond the hippocampal region.