High Gamma Oscillations Research Articles

MEG correlates of epileptic high gamma oscillations in invasive EEG

In patients with pharmacoresistant focal epilepsy,we demonstrate that magnetoencephalography (MEG) detects spike-locked and spike-independent epileptic high gamma oscillations (HGOs) using combined MEG and invasive electroencephalography (iEEG) from subdural macroelectrodes. Six patients, who underwent presurgical workup for epilepsy surgery with preoperative simultaneous MEG and subdural iEEG recordings,were investigated. HGOs in iEEG were detected automatically and served as triggers for averaging and localization of simultaneous MEG data. iEEG-HGOs were detected in all patients and MEG-HGOs in five patients. HGOs were highly associated with epileptic networks and correctly identified seizure-onset zones in five (MEG) and six patients (iEEG). Minimum-norm source analysis of MEG data yielded concordant localizations. Noninvasive analysis of HGOs may allow investigation of epileptic networks independent of spikes and seizures. Determination of sensitivity and specificity, as well as development of MEG-HGO analysis without the need of iEEG should be addressed in a larger study.

High Gamma Oscillations of Sensorimotor Cortex During Unilateral Movement in the Developing Brain: a MEG Study

Recent studies in adults have found consistent contralateral high gamma activities in the sensorimotor cortex during unilateral finger movement. However, no study has reported on this same phenomenon in children. We hypothesized that contralateral high gamma activities also exist in children during unilateral finger movement. Sixty normal children (6-17years old) were studied with a 275-channel MEG system combined with synthetic aperture magnetometry (SAM). Sixty participants displayed consistently contralateral event-related synchronization (C-ERS) within high gamma band (65-150Hz) in the primary motor cortices (M1) of both hemispheres. Interestingly, nineteen younger children displayed ipsilateral event-related synchronization (I-ERS) within the high gamma band (65-150Hz) just during their left finger movement. Both I-ERS and C-ERS were localized in M1. The incidence of I-ERS showed a significant decrease with age. Males had significantly higher odds of having ipsilateral activity compared to females. Noteworthy, high gamma C-ERS appeared consistently, while high gamma I-ERS changed with age. The asymmetrical patterns of neuromagnetic activities in the children's brain might represent the maturational lateralization and/or specialization of motor function. In conclusion, the present results have demonstrated that contralateral high-gamma neuromagnetic activities are potential biomarkers for the accurate localization of the primary motor cortex in children. In addition, the interesting finding of the ipsilateral high-gamma neuromagnetic activities opens a new window for us to understand the developmental changes of the hemispherical functional lateralization in the motor system.

Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep.

Gamma oscillations (40-120 Hz), usually associated with waking functions, can be recorded in the deepest stages of sleep in animals. The full details of their large-scale coordination across multiple cortical networks are still unknown. Furthermore, it is not known whether oscillations with similar characteristics are also present in the human brain. In this study, we examined the existence of gamma oscillations during polysomnographically defined sleep-wake states using large-scale microelectrode recordings (up to 56 channels), with single-cell and spike-time precision, in epilepsy patients. We report that low (40-80 Hz) and high (80-120 Hz) gamma oscillations recurrently emerged over time windows of several hundreds of milliseconds in all investigated cortical areas during slow-wave sleep. These patterns were correlated with positive peaks of EEG slow oscillations and marked increases in local cellular discharges, suggesting that they were associated with cortical UP states. These gamma oscillations frequently appeared at approximately the same time in many different cortical areas, including homotopic regions, forming large spatial patterns. Coincident firings with millisecond precision were strongly enhanced during gamma oscillations but only between cells within the same cortical area. Furthermore, in a significant number of cases, cortical gamma oscillations tended to occur within 100 ms after hippocampal ripple/sharp wave complexes. These data confirm and extend earlier animal studies reporting that gamma oscillations are transiently expressed during UP states during sleep. We speculate that these high-frequency patterns briefly restore "microwake" activity and are important for consolidation of memory traces acquired during previous awake periods.

Theta–gamma phase synchronization during memory matching in visual working memory

In most cases, object recognition is related to the matching of internal memory contents and bottom-up external sensory stimulation. The aim of this study was to investigate the electrophysiological correlates of memory matching based on EEG oscillatory phase synchronization analysis. Healthy subjects completed a delayed-match to sample task in which items stored in visual-spatial short-term memory had to be compared with a matching or non-matching probe. The results show that memory matching appears as transient phase-synchronization over parieto-occipital regions between theta (4–8Hz) and high gamma (50–70Hz) oscillations, 150–200ms post probe presentation. When memory representation and visual information match, phase-synchronization is stronger in the right hemisphere; conversely, when they do not match, stronger phase synchronization is observed in the left hemisphere. The present results reveal the integrative role of oscillatory activity in the memory matching process.

Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs

Oscillations may organize communication between components of large-scale brain networks. Although gamma-band oscillations have been repeatedly observed in cortical-basal ganglia circuits, their functional roles are not yet clear. Here I show that, in behaving rats, distinct frequencies of ventral striatal local field potential oscillations show coherence with different cortical inputs. The approximately 50 Hz gamma oscillations that normally predominate in awake ventral striatum are coherent with piriform cortex, whereas approximately 80-100 Hz high-gamma oscillations are coherent with frontal cortex. Within striatum, entrainment to gamma rhythms is selective to fast-spiking interneurons, with distinct fast-spiking interneuron populations entrained to different gamma frequencies. Administration of the psychomotor stimulant amphetamine or the dopamine agonist apomorphine causes a prolonged decrease in approximately 50 Hz power and increase in approximately 80-100 Hz power. The same frequency switch is observed for shorter epochs spontaneously in awake, undrugged animals and is consistently provoked for < 1 s following reward receipt. Individual striatal neurons can participate in these brief high-gamma bursts with, or without, substantial changes in firing rate. Switching between discrete oscillatory states may allow different modes of information processing during decision-making and reinforcement-based learning, and may also be an important systems-level process by which stimulant drugs affect cognition and behavior.

Detection of High Gamma Oscillations Associated with Visual Evoked Potentials is Improved by Independent Component Analysis

Detection of High Gamma Oscillations Associated with Visual Evoked Potentials is Improved by Independent Component Analysis

Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a learned spatial decision task

Local field potential (LFP) oscillations in the brain reflect organization thought to be important for perception, attention, movement, and memory. In the basal ganglia, including dorsal striatum, dysfunctional LFP states are associated with Parkinson's disease, while in healthy subjects, dorsal striatal LFPs have been linked to decision-making processes. However, LFPs in ventral striatum have been less studied. We report that in rats running a spatial decision task, prominent gamma-50 (45–55 Hz) and gamma-80 (70–85 Hz) oscillations in ventral striatum had distinct relationships to behavior, task events, and spiking activity. Gamma-50 power increased sharply following reward delivery and before movement initiation, while in contrast, gamma-80 power ramped up gradually to reward locations. Gamma-50 power was low and contained little structure during early learning, but rapidly developed a stable pattern, while gamma-80 power was initially high before returning to a stable level within a similar timeframe. Putative fast-spiking interneurons (FSIs) showed phase, firing rate, and coherence relationships with gamma-50 and gamma-80, indicating that the observed LFP patterns are locally relevant. Furthermore, in a number of FSIs such relationships were specific to gamma-50 or gamma-80, suggesting that partially distinct FSI populations mediate the effects of gamma-50 and gamma-80.

Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography

Recent studies using electrocorticographic (ECoG) recordings in humans have shown that functional activation of cortex is associated with an increase in power in the high-gamma frequency range ( approximately 60-200 Hz). Here we investigate the neural correlates of this high-gamma activity in local field potential (LFP). Single units and LFP were recorded with microelectrodes from the hand region of macaque secondary somatosensory cortex while vibrotactile stimuli of varying intensities were presented to the hand. We found that high-gamma power in the LFP was strongly correlated with the average firing rate recorded by the microelectrodes, both temporally and on a trial-by-trial basis. In comparison, the correlation between firing rate and low-gamma power (40-80 Hz) was much smaller. To explore the potential effects of neuronal firing on ECoG, we developed a model to estimate ECoG power generated by different firing patterns of the underlying cortical population and studied how ECoG power varies with changes in firing rate versus the degree of synchronous firing between neurons in the population. Both an increase in firing rate and neuronal synchrony increased high-gamma power in the simulated ECoG data. However, ECoG high-gamma activity was much more sensitive to increases in neuronal synchrony than firing rate.

Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex

Neuronal oscillations in the gamma frequency range have been reported in many cortical areas, but the role they play in cortical processing remains unclear. We tested a recently proposed hypothesis that the intensity of sensory input is coded in the timing of action potentials relative to the phase of gamma oscillations, thus converting amplitude information to a temporal code. We recorded spikes and local field potential (LFP) from secondary somatosensory (SII) cortex in awake monkeys while presenting a vibratory stimulus at different amplitudes. We developed a novel technique based on matching pursuit to study the interaction between the highly transient gamma oscillations and spikes with high time-frequency resolution. We found that spikes were weakly coupled to LFP oscillations in the gamma frequency range (40-80 Hz), and strongly coupled to oscillations in higher gamma frequencies. However, the phase relationship of neither low-gamma nor high-gamma oscillations changed with stimulus intensity, even with a 10-fold increase. We conclude that, in SII, gamma oscillations are synchronized with spikes, but their phase does not vary with stimulus intensity. Furthermore, high-gamma oscillations (>60 Hz) appear to be closely linked to the occurrence of action potentials, suggesting that LFP high-gamma power could be a sensitive index of the population firing rate near the microelectrode.

High-frequency oscillations in distributed neural networks reveal the dynamics of human decision making

We examine the relative timing of numerous brain regions involved in human decisions that are based on external criteria, learned information, personal preferences, or unconstrained internal considerations. Using magnetoencephalography (MEG) and advanced signal analysis techniques, we were able to non-invasively reconstruct oscillations of distributed neural networks in the high-gamma frequency band (60–150 Hz). The time course of the observed neural activity suggested that two-alternative forced choice tasks are processed in four overlapping stages: processing of sensory input, option evaluation, intention formation, and action execution. Visual areas are activated first, and show recurring activations throughout the entire decision process. The temporo-occipital junction and the intraparietal sulcus are active during evaluation of external values of the options, 250–500 ms after stimulus presentation. Simultaneously, personal preference is mediated by cortical midline structures. Subsequently, the posterior parietal and superior occipital cortices appear to encode intention, with different subregions being responsible for different types of choice. The cerebellum and inferior parietal cortex are recruited for internal generation of decisions and actions, when all options have the same value. Action execution was accompanied by activation peaks in the contralateral motor cortex. These results suggest that high-gamma oscillations as recorded by MEG allow a reliable reconstruction of decision processes with excellent spatiotemporal resolution.

Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex

Rapid optimization of behavior requires decisions about when to explore and when to exploit discovered resources. The mechanisms that lead to fast adaptations and their interaction with action valuation are a central issue. We show here that the anterior cingulate cortex (ACC) encodes multiple feedbacks devoted to exploration and its immediate termination. In a task that alternates exploration and exploitation periods, the ACC monitored negative and positive outcomes relevant for different adaptations. In particular, it produced signals specific of the first reward, i.e., the end of exploration. Those signals disappeared in exploitation periods but immediately transferred to the initiation of trials-a transfer comparable to learning phenomena observed for dopaminergic neurons. Importantly, these were also observed for high gamma oscillations of local field potentials shown to correlate with brain imaging signal. Thus, mechanisms of action valuation and monitoring of events/actions are combined for rapid behavioral regulation.

A Blueprint for Real-Time Functional Mapping via Human Intracranial Recordings

BackgroundThe surgical treatment of patients with intractable epilepsy is preceded by a pre-surgical evaluation period during which intracranial EEG recordings are performed to identify the epileptogenic network and provide a functional map of eloquent cerebral areas that need to be spared to minimize the risk of post-operative deficits. A growing body of research based on such invasive recordings indicates that cortical oscillations at various frequencies, especially in the gamma range (40 to 150 Hz), can provide efficient markers of task-related neural network activity.Principal FindingsHere we introduce a novel real-time investigation framework for mapping human brain functions based on online visualization of the spectral power of the ongoing intracranial activity. The results obtained with the first two implanted epilepsy patients who used the proposed online system illustrate its feasibility and utility both for clinical applications, as a complementary tool to electrical stimulation for presurgical mapping purposes, and for basic research, as an exploratory tool used to detect correlations between behavior and oscillatory power modulations. Furthermore, our findings suggest a putative role for high gamma oscillations in higher-order auditory processing involved in speech and music perception.Conclusion/SignificanceThe proposed real-time setup is a promising tool for presurgical mapping, the investigation of functional brain dynamics, and possibly for neurofeedback training and brain computer interfaces.

Olfactory Bulb Gamma Oscillations Are Enhanced with Task Demands

Fast oscillations in neural assemblies have been proposed as a mechanism to facilitate stimulus representation in a variety of sensory systems across animal species. In the olfactory system, intervention studies suggest that oscillations in the gamma frequency range play a role in fine odor discrimination. However, there is still no direct evidence that such oscillations are intrinsically altered in intact systems to aid in stimulus disambiguation. Here we show that gamma oscillatory power in the rat olfactory bulb during a two-alternative choice task is modulated in the intact system according to task demands with dramatic increases in gamma power during discrimination of molecularly similar odorants in contrast to dissimilar odorants. This elevation in power evolves over the course of criterion performance, is specific to the gamma frequency band (65-85 Hz), and is independent of changes in the theta or beta frequency band range. Furthermore, these high amplitude gamma oscillations are restricted to the olfactory bulb, such that concurrent piriform cortex recordings show no evidence of enhanced gamma power during these high-amplitude events. Our results display no modulation in the power of beta oscillations (15-28 Hz) shown previously to increase with odor learning in a Go/No-go task, and we suggest that the oscillatory profile of the olfactory system may be influenced by both odor discrimination demands and task type. The results reported here indicate that enhancement of local gamma power may reflect a switch in the dynamics of the system to a strategy that optimizes stimulus resolution when input signals are ambiguous.

Working memory related gamma oscillations in schizophrenia patients

Recent reports show that the capability of neural networks supporting high-frequency synchronization is reduced in the brain of schizophrenia patients. Specifically, deficits in gamma activity have been shown in schizophrenia patients during perception and simple cognitive tasks. However little is known about alterations in gamma responses during complex and higher cognitive processing. The main objective of this study was to investigate modulation of event-related gamma responses in tasks varying working memory (WM) load in schizophrenia patients ( N = 10) and healthy controls ( N = 10). Gamma amplitude values were obtained for a simple choice reaction task, a low WM demand task, and a high WM demand task. During all three tasks schizophrenia patients showed significantly slower reaction times and higher error rates than controls. A gradual increase of gamma amplitudes after stimulus onset was associated with increase of WM load in controls. In contrast, high amplitude gamma oscillations remained constant regardless of task difficulty in patients. These results suggest that healthy subjects used various cognitive strategies depending on task difficulty, while schizophrenia patients needed to initiate complex cognitive processes similar to those used during processing of novel contexts or stimuli even for the simple choice reaction task with low cognitive demand.

High Gamma Activity in Response to Deviant Auditory Stimuli Recorded Directly From Human Cortex

We recorded electrophysiological responses from the left frontal and temporal cortex of awake neurosurgical patients to both repetitive background and rare deviant auditory stimuli. Prominent sensory event-related potentials (ERPs) were recorded from auditory association cortex of the temporal lobe and adjacent regions surrounding the posterior Sylvian fissure. Deviant stimuli generated an additional longer latency mismatch response, maximal at more anterior temporal lobe sites. We found low gamma (30-60 Hz) in auditory association cortex, and we also show the existence of high-frequency oscillations above the traditional gamma range (high gamma, 60-250 Hz). Sensory and mismatch potentials were not reliably observed at frontal recording sites. We suggest that the high gamma oscillations are sensory-induced neocortical ripples, similar in physiological origin to the well-studied ripples of the hippocampus.

Neuromagnetic gamma-band activity in the primary and secondary somatosensory areas.

To evaluate the gamma-band activity related to somatosensory processing, we recorded neuromagnetic signals from seven healthy subjects. The source power changes evoked by electrical stimulation of the median nerve were estimated with synthetic aperture magnetometry (SAM). Source power in the low gamma band (40 Hz) decreased in the contralateral primary somatosensory cortex (SI) for a few hundred milliseconds (i.e. middle and long latency) and then increased inversely. Source power in the high gamma band (70-90 Hz) increased simultaneously both in the contralateral SI and contra/ipsilateral secondary somatosensory cortex (SII) in 80-180 ms. These results suggest that low and high gamma oscillations work under independent mechanisms during somatosensory processing. In particular, high gamma oscillations may play an essential role in making a functional connection between SI and SII.

Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: role of fast NMDA channels.

Recordings from brain regions involved in memory function show dual oscillations in which each cycle of a low-frequency theta oscillation (5-8 Hz) is subdivided into about seven subcycles by high frequency gamma oscillations (20-60 Hz). It has been proposed (Lisman and Idiart 1995) that such networks are a multiplexed short-term memory (STM) buffer that can actively maintain about seven memories, a capability of human STM. A memory is encoded by a subset of principal neurons that fire synchronously in a particular gamma subcycle. Firing is maintained by a membrane process intrinsic to each cell. We now extend this model by incorporating recurrent connections with modifiable synapses to store long-term memory (LTM). The repetition provided by STM gradually modifies synapses in a physiologically realistic way. Because different memories are active in different gamma subcycles, the formation of autoassociative LTM requires that synaptic modification depend on N-methyl-D-aspartate (NMDA) channels having a time constant of deactivation that is of the same order as the duration of a gamma subcycle (15-50 msec). Many types of NMDA channels have longer time constants (150 msec), as for instance those found in the hippocampus, but both fast and slow NMDA channels are present in cortex. This is the first proposal for the special role of these fast NMDA channels. The STM for novel items must depend on activity-dependent changes intrinsic to neurons rather than recurrent connections, which have not developed the required selectivity. Because these intrinsic mechanisms are not error-correcting, STM will become slowly corrupted by noise. This limits the accuracy with which LTM can become encoded after a single presentation. Accurate encoding of items in LTM can be achieved by multiple presentations, provided different memory items are presented in a varied interleaved order. Our results indicate that a limited memory-capacity STM model can be integrated in the same network with a high-capacity LTM model.