Gamma oscillations in human primary somatosensory cortex reflect pain perception

Successful behavior requires selection and preferred processing of relevant sensory information. The cortical representation of relevant sensory information has been related to neuronal oscillations in the gamma frequency band. Pain is of invariably high behavioral relevance and, thus, nociceptive stimuli receive preferred processing. Here, by using magnetoencephalography, we show that selective nociceptive stimuli induce gamma oscillations between 60 and 95 Hz in primary somatosensory cortex. Amplitudes of pain-induced gamma oscillations vary with objective stimulus intensity and subjective pain intensity. However, around pain threshold, perceived stimuli yielded stronger gamma oscillations than unperceived stimuli of equal stimulus intensity. These results show that pain induces gamma oscillations in primary somatosensory cortex that are particularly related to the subjective perception of pain. Our findings support the hypothesis that gamma oscillations are related to the internal representation of behaviorally relevant stimuli that should receive preferred processing.     

Human gamma oscillations during slow wave sleep

Neocortical local field potentials have shown that gamma oscillations occur spontaneously during slow-wave sleep (SWS). At the macroscopic EEG level in the human brain, no evidences were reported so far. In this study, by using simultaneous scalp and intracranial EEG recordings in 20 epileptic subjects, we examined gamma oscillations in cerebral cortex during SWS. We report that gamma oscillations in low (30-50 Hz) and high (60-120 Hz) frequency bands recurrently emerged in all investigated regions and their amplitudes coincided with specific phases of the cortical slow wave. In most of the cases, multiple oscillatory bursts in different frequency bands from 30 to 120 Hz were correlated with positive peaks of scalp slow waves ("IN-phase" pattern), confirming previous animal findings. In addition, we report another gamma pattern that appears preferentially during the negative phase of the slow wave ("ANTI-phase" pattern). This new pattern presented dominant peaks in the high gamma range and was preferentially expressed in the temporal cortex. Finally, we found that the spatial coherence between cortical sites exhibiting gamma activities was local and fell off quickly when computed between distant sites. Overall, these results provide the first human evidences that gamma oscillations can be observed in macroscopic EEG recordings during sleep. They support the concept that these high-frequency activities might be associated with phasic increases of neural activity during slow oscillations. Such patterned activity in the sleeping brain could play a role in off-line processing of cortical networks.     

Input-Dependent Frequency Modulation of Cortical Gamma Oscillations Shapes Spatial Synchronization and Enables Phase Coding

Fine-scale temporal organization of cortical activity in the gamma range (∼25–80Hz) may play a significant role in information processing, for example by neural grouping (‘binding’) and phase coding. Recent experimental studies have shown that the precise frequency of gamma oscillations varies with input drive (e.g. visual contrast) and that it can differ among nearby cortical locations. This has challenged theories assuming widespread gamma synchronization at a fixed common frequency. In the present study, we investigated which principles govern gamma synchronization in the presence of input-dependent frequency modulations and whether they are detrimental for meaningful input-dependent gamma-mediated temporal organization. To this aim, we constructed a biophysically realistic excitatory-inhibitory network able to express different oscillation frequencies at nearby spatial locations. Similarly to cortical networks, the model was topographically organized with spatially local connectivity and spatially-varying input drive. We analyzed gamma synchronization with respect to phase-locking, phase-relations and frequency differences, and quantified the stimulus-related information represented by gamma phase and frequency. By stepwise simplification of our models, we found that the gamma-mediated temporal organization could be reduced to basic synchronization principles of weakly coupled oscillators, where input drive determines the intrinsic (natural) frequency of oscillators. The gamma phase-locking, the precise phase relation and the emergent (measurable) frequencies were determined by two principal factors: the detuning (intrinsic frequency difference, i.e. local input difference) and the coupling strength. In addition to frequency coding, gamma phase contained complementary stimulus information. Crucially, the phase code reflected input differences, but not the absolute input level. This property of relative input-to-phase conversion, contrasting with latency codes or slower oscillation phase codes, may resolve conflicting experimental observations on gamma phase coding. Our modeling results offer clear testable experimental predictions. We conclude that input-dependency of gamma frequencies could be essential rather than detrimental for meaningful gamma-mediated temporal organization of cortical activity.     

Electrical Brain Responses to an Auditory Illusion and the Impact of Musical Expertise

The presentation of two sinusoidal tones, one to each ear, with a slight frequency mismatch yields an auditory illusion of a beating frequency equal to the frequency difference between the two tones; this is known as binaural beat (BB). The effect of brief BB stimulation on scalp EEG is not conclusively demonstrated. Further, no studies have examined the impact of musical training associated with BB stimulation, yet musicians'' brains are often associated with enhanced auditory processing. In this study, we analysed EEG brain responses from two groups, musicians and non-musicians, when stimulated by short presentation (1 min) of binaural beats with beat frequency varying from 1 Hz to 48 Hz. We focused our analysis on alpha and gamma band EEG signals, and they were analysed in terms of spectral power, and functional connectivity as measured by two phase synchrony based measures, phase locking value and phase lag index. Finally, these measures were used to characterize the degree of centrality, segregation and integration of the functional brain network. We found that beat frequencies belonging to alpha band produced the most significant steady-state responses across groups. Further, processing of low frequency (delta, theta, alpha) binaural beats had significant impact on cortical network patterns in the alpha band oscillations. Altogether these results provide a neurophysiological account of cortical responses to BB stimulation at varying frequencies, and demonstrate a modulation of cortico-cortical connectivity in musicians'' brains, and further suggest a kind of neuronal entrainment of a linear and nonlinear relationship to the beating frequencies.     

Selective coupling between theta phase and neocortical fast gamma oscillations during REM-sleep in mice

Background

The mammalian brain expresses a wide range of state-dependent network oscillations which vary in frequency and spatial extension. Such rhythms can entrain multiple neurons into coherent patterns of activity, consistent with a role in behaviour, cognition and memory formation. Recent evidence suggests that locally generated fast network oscillations can be systematically aligned to long-range slow oscillations. It is likely that such cross-frequency coupling supports specific tasks including behavioural choice and working memory.

Principal Findings

We analyzed temporal coupling between high-frequency oscillations and EEG theta activity (4–12 Hz) in recordings from mouse parietal neocortex. Theta was exclusively present during active wakefulness and REM-sleep. Fast oscillations occurred in two separate frequency bands: gamma (40–100 Hz) and fast gamma (120–160 Hz). Theta, gamma and fast gamma were more prominent during active wakefulness as compared to REM-sleep. Coupling between theta and the two types of fast oscillations, however, was more pronounced during REM-sleep. This state-dependent cross-frequency coupling was particularly strong for theta-fast gamma interaction which increased 9-fold during REM as compared to active wakefulness. Theta-gamma coupling increased only by 1.5-fold.

Significance

State-dependent cross-frequency-coupling provides a new functional characteristic of REM-sleep and establishes a unique property of neocortical fast gamma oscillations. Interactions between defined patterns of slow and fast network oscillations may serve selective functions in sleep-dependent information processing.     

Driving oscillatory activity in the human cortex enhances motor performance

Voluntary movement is accompanied by changes in the degree to which neurons in the brain synchronize their activity within discrete frequency ranges. Two patterns of movement-related oscillatory activity stand out in human cortical motor areas. Activity in the beta frequency (15-30 Hz) band is prominent during tonic contractions but is attenuated prior to and during voluntary movement. Without such attenuation, movement may be slowed, leading to the suggestion that beta activity promotes postural and tonic contraction, possibly at a cost to the generation of new movements. In contrast, activity in the gamma (60-90 Hz) band increases during movement. The direction of change suggests that gamma activity might facilitate motor processing. In correspondence with this, increased frontal gamma activity is related with reduced reaction times. Yet the possibility remains that these functional correlations reflect an epiphenomenal rather than causal relationship. Here we provide strong evidence that oscillatory activities at the cortical level are mechanistically involved in determining motor behavior and can even improve performance. By driving cortical oscillations using noninvasive electrical stimulation, we show opposing effects at beta and gamma frequencies and interactions with motor task that reveal the potential quantitative importance of oscillations in motor behavior.     

Role of frequency mismatch in neuronal communication through coherence

Neuronal gamma oscillations have been described in local field potentials of different brain regions of multiple species. Gamma oscillations are thought to reflect rhythmic synaptic activity organized by inhibitory interneurons. While several aspects of gamma rhythmogenesis are relatively well understood, we have much less solid evidence about how gamma oscillations contribute to information processing in neuronal circuits. One popular hypothesis states that a flexible routing of information between distant populations occurs via the control of the phase or coherence between their respective oscillations. Here, we investigate how a mismatch between the frequencies of gamma oscillations from two populations affects their interaction. In particular, we explore a biophysical model of the reciprocal interaction between two cortical areas displaying gamma oscillations at different frequencies, and quantify their phase coherence and communication efficiency. We observed that a moderate excitatory coupling between the two areas leads to a decrease in their frequency detuning, up to ～6 Hz, with no frequency locking arising between the gamma peaks. Importantly, for similar gamma peak frequencies a zero phase difference emerges for both LFP and MUA despite small axonal delays. For increasing frequency detunings we found a significant decrease in the phase coherence (at non-zero phase lag) between the MUAs but not the LFPs of the two areas. Such difference between LFPs and MUAs behavior is due to the misalignment between the arrival of afferent synaptic currents and the local excitability windows. To test the efficiency of communication we evaluated the success of transferring rate-modulations between the two areas. Our results indicate that once two populations lock their peak frequencies, an optimal phase relation for communication appears. However, the sensitivity of locking to frequency mismatch suggests that only a precise and active control of gamma frequency could enable the selection of communication channels and their directionality.     

Long lasting modulation of cortical oscillations after continuous theta burst transcranial magnetic stimulation

Transcranial magnetic theta burst stimulation (TBS) differs from other high-frequency rTMS protocols because it induces plastic changes up to an hour despite lower stimulus intensity and shorter duration of stimulation. However, the effects of TBS on neuronal oscillations remain unclear. In this study, we used electroencephalography (EEG) to investigate changes of neuronal oscillations after continuous TBS (cTBS), the protocol that emulates long-term depression (LTD) form of synaptic plasticity. We randomly divided 26 healthy humans into two groups receiving either Active or Sham cTBS as control over the left primary motor cortex (M1). Post-cTBS aftereffects were assessed with behavioural measurements at rest using motor evoked potentials (MEPs) and at active state during the execution of a choice reaction time (RT) task in combination with continuous electrophysiological recordings. The cTBS-induced EEG oscillations were assessed using event-related power (ERPow), which reflected regional oscillatory activity of neural assemblies of θ (4-7.5 Hz), low α (8-9.5 Hz), μ (10-12.5 Hz), low β (13-19.5 Hz), and high β (20-30 Hz) brain rhythms. Results revealed 20-min suppression of MEPs and at least 30-min increase of ERPow modulation, suggesting that besides MEPs, EEG has the potential to provide an accurate cortical readout to assess cortical excitability and to investigate the interference of cortical oscillations in the human brain post-cTBS. We also observed a predominant modulation of β frequency band, supporting the hypothesis that cTBS acts more on cortical level. Theta oscillations were also modulated during rest implying the involvement of independent cortical theta generators over the motor network post cTBS. This work provided more insights into the underlying mechanisms of cTBS, providing a possible link between synchronised neural oscillations and LTD in humans.     

Gamma Activity Coupled to Alpha Phase as a Mechanism for Top-Down Controlled Gating

Coupling between neural oscillations in different frequency bands has been proposed to coordinate neural processing. In particular, gamma power coupled to alpha phase is proposed to reflect gating of information in the visual system but the existence of such a mechanism remains untested. Here, we recorded ongoing brain activity using magnetoencephalography in subjects who performed a modified Sternberg working memory task in which distractors were presented in the retention interval. During the anticipatory pre-distractor period, we show that the phase of alpha oscillations was coupled with the power of high (80-120Hz) gamma band activity, i.e. gamma power consistently was lower at the trough than at the peak of the alpha cycle (9-12Hz). We further show that high alpha power was associated with weaker gamma power at the trough of the alpha cycle. This result is in line with alpha activity in sensory region implementing a mechanism of pulsed inhibition silencing neuronal firing every ~100 ms.     

Respiration modulates oscillatory neural network activity at rest

Despite recent advances in understanding how respiration affects neural signalling to influence perception, cognition, and behaviour, it is yet unclear to what extent breathing modulates brain oscillations at rest. We acquired respiration and resting state magnetoencephalography (MEG) data from human participants to investigate if, where, and how respiration cyclically modulates oscillatory amplitudes (2 to 150 Hz). Using measures of phase–amplitude coupling, we show respiration-modulated brain oscillations (RMBOs) across all major frequency bands. Sources of these modulations spanned a widespread network of cortical and subcortical brain areas with distinct spectrotemporal modulation profiles. Globally, delta and gamma band modulations varied with distance to the head centre, with stronger modulations at distal (versus central) cortical sites. Overall, we provide the first comprehensive mapping of RMBOs across the entire brain, highlighting respiration–brain coupling as a fundamental mechanism to shape neural processing within canonical resting state and respiratory control networks (RCNs).

Despite recent advances, it remains unclear to what extent breathing modulates brain oscillations at rest. This magnetoencephalography study in human participants identifies a widespread brain network of neural oscillations that are coupled to the respiratory rhythm.     

The visual cortex produces gamma band echo in response to broadband visual flicker

The aim of this study is to uncover the network dynamics of the human visual cortex by driving it with a broadband random visual flicker. We here applied a broadband flicker (1–720 Hz) while measuring the MEG and then estimated the temporal response function (TRF) between the visual input and the MEG response. This TRF revealed an early response in the 40–60 Hz gamma range as well as in the 8–12 Hz alpha band. While the gamma band response is novel, the latter has been termed the alpha band perceptual echo. The gamma echo preceded the alpha perceptual echo. The dominant frequency of the gamma echo was subject-specific thereby reflecting the individual dynamical properties of the early visual cortex. To understand the neuronal mechanisms generating the gamma echo, we implemented a pyramidal-interneuron gamma (PING) model that produces gamma oscillations in the presence of constant input currents. Applying a broadband input current mimicking the visual stimulation allowed us to estimate TRF between the input current and the population response (akin to the local field potentials). The TRF revealed a gamma echo that was similar to the one we observed in the MEG data. Our results suggest that the visual gamma echo can be explained by the dynamics of the PING model even in the absence of sustained gamma oscillations.     

Selective Modulation of Interhemispheric Functional Connectivity by HD-tACS Shapes Perception

Oscillatory neuronal synchronization between cortical areas has been suggested to constitute a flexible mechanism to coordinate information flow in the human cerebral cortex. However, it remains unclear whether synchronized neuronal activity merely represents an epiphenomenon or whether it is causally involved in the selective gating of information. Here, we combined bilateral high-density transcranial alternating current stimulation (HD-tACS) at 40 Hz with simultaneous electroencephalographic (EEG) recordings to study immediate electrophysiological effects during the selective entrainment of oscillatory gamma-band signatures. We found that interhemispheric functional connectivity was modulated in a predictable, phase-specific way: In-phase stimulation enhanced synchronization, anti-phase stimulation impaired functional coupling. Perceptual correlates of these connectivity changes were found in an ambiguous motion task, which strongly support the functional relevance of long-range neuronal coupling. Additionally, our results revealed a decrease in oscillatory alpha power in response to the entrainment of gamma band signatures. This finding provides causal evidence for the antagonistic role of alpha and gamma oscillations in the parieto-occipital cortex and confirms that the observed gamma band modulations were physiological in nature. Our results demonstrate that synchronized cortical network activity across several spatiotemporal scales is essential for conscious perception and cognition.     

Spontaneously active cells induce state transitions in a model of olfactory cortex

The existence of neurons with intrinsic oscillations does not in itself explain the synchronization of local populations of neurons, but it is likely to pace population rhythms when the neurons are suitably coupled by chemical and/or electrical synapses. In the present study, we have investigated the role of spontaneously active cells as noisy or pacemaker units in setting global oscillations in a three-layered cortical model. The presence of a small number of noisy (spontaneously active) units induce oscillations at the network level in the range of the gamma rhythm. The number of noisy units in the network and their type (excitatory or inhibitory or excitatory and inhibitory together) determines the emergence of regular oscillations or aperiodic (chaotic) behaviour. It also determines the onset of the global behaviour. On replacing a noisy unit by a pacemaker unit, similar gamma oscillations were generated. With both noisy and pacemaker units, we found that certain characteristics of the spontaneous activity determine the delay period for the onset of global activity. Preliminary studies have been carried out with spontaneously active units having a chaotic dynamics but the results are much similar to that with a noisy burst. Different functional roles have been suggested for cortical oscillations, such as determining global functional states and specifying connectivity during development. Oscillations at different frequency bands, in particular in the gamma band (around 40 Hz), have also been associated with memory and attention. The presence of spontaneously active neurons, either with noisy or oscillatory activity, could be responsible for global oscillations in the absence of external stimuli in certain cortical areas in the mature brain.     

Functional dissociation of ongoing oscillatory brain states

The state of a neural assembly preceding an incoming stimulus is assumed to modulate the processing of subsequently presented stimuli. The nature of this state can differ with respect to the frequency of ongoing oscillatory activity. Oscillatory brain activity of specific frequency range such as alpha (8-12 Hz) and gamma (above 30 Hz) band oscillations are hypothesized to play a functional role in cognitive processing. Therefore, a selective modulation of this prestimulus activity could clarify the functional role of these prestimulus fluctuations. For this purpose, we adopted a novel non-invasive brain-computer-interface (BCI) strategy to selectively increase alpha or gamma band activity in the occipital cortex combined with an adaptive presentation of visual stimuli within specific brain states. During training, oscillatory brain activity was estimated online and fed back to the participants to enable a deliberate modulation of alpha or gamma band oscillations. Results revealed that volunteers selectively increased alpha and gamma frequency oscillations with a high level of specificity regarding frequency range and localization. At testing, alpha or gamma band activity was classified online and at defined levels of activity, visual objects embedded in noise were presented instantly and had to be detected by the volunteer. In experiment I, the effect of two levels of prestimulus gamma band activity on visual processing was examined. During phases of increased gamma band activity significantly more visual objects were detected. In experiment II, the effect was compared against increased levels of alpha band activity. An improvement of visual processing was only observed for enhanced gamma band activity. Both experiments demonstrate the specific functional role of prestimulus gamma band oscillations for perceptual processing. We propose that the BCI method permits the selective modulation of oscillatory activity and the direct assessment of behavioral consequences to test for functional dissociations of different oscillatory brain states.     

Different origins of gamma rhythm and high-gamma activity in macaque visual cortex

During cognitive tasks electrical activity in the brain shows changes in power in specific frequency ranges, such as the alpha (8-12 Hz) or gamma (30-80 Hz) bands, as well as in a broad range above ～80 Hz, called the high-gamma band. The role or significance of this broadband high-gamma activity is unclear. One hypothesis states that high-gamma oscillations serve just like gamma oscillations, operating at a higher frequency and consequently at a faster timescale. Another hypothesis states that high-gamma power is related to spiking activity. Because gamma power and spiking activity tend to co-vary during most stimulus manipulations (such as contrast modulations) or cognitive tasks (such as attentional modulation), it is difficult to dissociate these two hypotheses. We studied the relationship between high-gamma power, gamma rhythm, and spiking activity in the primary visual cortex (V1) of awake monkeys while varying the stimulus size, which increased the gamma power but decreased the firing rate, permitting a dissociation. We found that gamma power became anti-correlated with the high-gamma power, suggesting that the two phenomena are distinct and have different origins. On the other hand, high-gamma power remained tightly correlated with spiking activity under a wide range of stimulus manipulations. We studied this relationship using a signal processing technique called Matching Pursuit and found that action potentials are associated with sharp transients in the LFP with broadband power, which is visible at frequencies as low as ～50 Hz. These results distinguish broadband high-gamma activity from gamma rhythms as an easily obtained and reliable electrophysiological index of neuronal firing near the microelectrode. Further, they highlight the importance of making a careful dissociation between gamma rhythms and spike-related transients that could be incorrectly decomposed as rhythms using traditional signal processing methods.     

A new look at gamma? High- (>60 Hz) γ-band activity in cortical networks: function, mechanisms and impairment

γ-band oscillations are thought to play a crucial role in information processing in cortical networks. In addition to oscillatory activity between 30 and 60 Hz, current evidence from electro- and magnetoencephalography (EEG/MEG) and local-field potentials (LFPs) has consistently shown oscillations >60 Hz (high γ-band) whose function and generating mechanisms are unclear. In the present paper, we summarize data that highlights the importance of high γ-band activity for cortical computations through establishing correlations between the modulation of oscillations in the 60-200 Hz frequency and specific cognitive functions. Moreover, we will suggest that high γ-band activity is impaired in neuropsychiatric disorders, such as schizophrenia and epilepsy. In the final part of the paper, we will review physiological mechanisms underlying the generation of high γ-band oscillations and discuss the functional implications of low vs. high γ-band activity patterns in cortical networks.     

Death of Neurons following Injury Requires Conductive Neuronal Gap Junction Channels but Not a Specific Connexin

Pharmacological blockade or genetic knockout of neuronal connexin 36 (Cx36)-containing gap junctions reduces neuronal death caused by ischemia, traumatic brain injury and NMDA receptor (NMDAR)-mediated excitotoxicity. However, whether Cx36 gap junctions contribute to neuronal death via channel-dependent or channel-independent mechanism remains an open question. To address this, we manipulated connexin protein expression via lentiviral transduction of mouse neuronal cortical cultures and analyzed neuronal death twenty-four hours following administration of NMDA (a model of NMDAR excitotoxicity) or oxygen-glucose deprivation (a model of ischemic injury). In cultures prepared from wild-type mice, over-expression and knockdown of Cx36-containing gap junctions augmented and prevented, respectively, neuronal death from NMDAR-mediated excitotoxicity and ischemia. In cultures obtained form from Cx36 knockout mice, re-expression of functional gap junction channels, containing either neuronal Cx36 or non-neuronal Cx43 or Cx31, resulted in increased neuronal death following insult. In contrast, the expression of communication-deficient gap junctions (containing mutated connexins) did not have this effect. Finally, the absence of ethidium bromide uptake in non-transduced wild-type neurons two hours following NMDAR excitotoxicity or ischemia suggested the absence of active endogenous hemichannels in those neurons. Taken together, these results suggest a role for neuronal gap junctions in cell death via a connexin type-independent mechanism that likely relies on channel activities of gap junctional complexes among neurons. A possible contribution of gap junction channel-permeable death signals in neuronal death is discussed.     

A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities

Network oscillations support transient communication across brain structures. We show here, in rats, that task-related neuronal activity in the medial prefrontal cortex (PFC), the hippocampus, and the ventral tegmental area (VTA), regions critical for working memory, is coordinated by a 4 Hz oscillation. A prominent increase of power and coherence of the 4 Hz oscillation in the PFC and the VTA and its phase modulation of gamma power in both structures was present in the working memory part of the task. Subsets of both PFC and hippocampal neurons predicted the turn choices of the rat. The goal-predicting PFC pyramidal neurons were more strongly phase locked to both 4 Hz and hippocampal theta oscillations than nonpredicting cells. The 4 Hz and theta oscillations were phase coupled and jointly modulated both gamma waves and neuronal spikes in the PFC, the VTA, and the hippocampus. Thus, multiplexed timing mechanisms in the PFC-VTA-hippocampus axis may support processing of information, including working memory.     

Gamma Power Is Phase-Locked to Posterior Alpha Activity

Neuronal oscillations in various frequency bands have been reported in numerous studies in both humans and animals. While it is obvious that these oscillations play an important role in cognitive processing, it remains unclear how oscillations in various frequency bands interact. In this study we have investigated phase to power locking in MEG activity of healthy human subjects at rest with their eyes closed. To examine cross-frequency coupling, we have computed coherence between the time course of the power in a given frequency band and the signal itself within every channel. The time-course of the power was calculated using a sliding tapered time window followed by a Fourier transform. Our findings show that high-frequency gamma power (30–70 Hz) is phase-locked to alpha oscillations (8–13 Hz) in the ongoing MEG signals. The topography of the coupling was similar to the topography of the alpha power and was strongest over occipital areas. Interestingly, gamma activity per se was not evident in the power spectra and only became detectable when studied in relation to the alpha phase. Intracranial data from an epileptic subject confirmed these findings albeit there was slowing in both the alpha and gamma band. A tentative explanation for this phenomenon is that the visual system is inhibited during most of the alpha cycle whereas a burst of gamma activity at a specific alpha phase (e.g. at troughs) reflects a window of excitability.     

Specific Entrainment of Mitral Cells during Gamma Oscillation in the Rat Olfactory Bulb

Local field potential (LFP) oscillations are often accompanied by synchronization of activity within a widespread cerebral area. Thus, the LFP and neuronal coherence appear to be the result of a common mechanism that underlies neuronal assembly formation. We used the olfactory bulb as a model to investigate: (1) the extent to which unitary dynamics and LFP oscillations can be correlated and (2) the precision with which a model of the hypothesized underlying mechanisms can accurately explain the experimental data. For this purpose, we analyzed simultaneous recordings of mitral cell (MC) activity and LFPs in anesthetized and freely breathing rats in response to odorant stimulation. Spike trains were found to be phase-locked to the gamma oscillation at specific firing rates and to form odor-specific temporal patterns. The use of a conductance-based MC model driven by an approximately balanced excitatory-inhibitory input conductance and a relatively small inhibitory conductance that oscillated at the gamma frequency allowed us to provide one explanation of the experimental data via a mode-locking mechanism. This work sheds light on the way network and intrinsic MC properties participate in the locking of MCs to the gamma oscillation in a realistic physiological context and may result in a particular time-locked assembly. Finally, we discuss how a self-synchronization process with such entrainment properties can explain, under experimental conditions: (1) why the gamma bursts emerge transiently with a maximal amplitude position relative to the stimulus time course; (2) why the oscillations are prominent at a specific gamma frequency; and (3) why the oscillation amplitude depends on specific stimulus properties. We also discuss information processing and functional consequences derived from this mechanism.