Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system

Rojas‐Líbano, Daniel; Kay, Leslie M.

doi:10.1007/s11571-008-9053-1

Cited by 101 publications

(93 citation statements)

References 86 publications

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“…Differences between odor and prestimulus periods could be seen in the power of gamma band coherence within sites. This is consistent with the idea that gamma oscillations represent local processing of odor-specific information (Kay et al 2009;Rojas-Líbano and Kay 2008).…”

Section: Discussionsupporting

confidence: 91%

How Global Are Olfactory Bulb Oscillations?

Kay

Lazzara

2010

Journal of Neurophysiology

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Previous studies in waking animals have shown that the frequency structure of olfactory bulb (OB) local field potential oscillations is very similar across the OB, but large low-impedance surface electrodes may have favored highly coherent events, averaging out local inhomogeneities. We tested the hypothesis that OB oscillations represent spatially homogeneous phenomena at all scales. We used pairs of concentric electrodes (200 μm outer shaft surrounding an inner 2-3 μm recording site) beginning on the dorsal OB at anterior and medial locations in urethane-anesthetized rats and measured local field potential responses at successive 200 μm depths before and during odor stimulation. Within locations (outer vs. inner lead on a single probe), on the time scale of 0.5 s, coherence in all frequency bands was significant, but on larger time scales (10 s), only respiratory (1-4 Hz) and beta (15-30 Hz) oscillations showed prominent peaks. Across locations, coherence in all frequency bands was significantly lower for both sizes of electrodes at all depths but the most superficial 600 μm. Near the pial surface, coherence across outer (larger) electrodes at different sites was equal to coherence across outer and inner (small) electrodes within a single site and larger than coherence across inner electrodes at different sites. Overall, the beta band showed the largest coherence across bulbar sites and electrodes. Therefore larger electrodes at the surface of the OB favor globally coherent events, and at all depths, coherence depends on the type of oscillation (beta or gamma) and duration of the analysis window.

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Section: Discussionsupporting

confidence: 91%

How Global Are Olfactory Bulb Oscillations?

Kay

Lazzara

2010

Journal of Neurophysiology

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“…In the OB, the LFP signals in different frequencies (Fig. 1A) have different origins, amplitudes, and functions (22)(23)(24)(25). The GCL contains a large amount of local neurons whose dendrites radiate almost exclusively toward the more superficial external plexiform layer, generating the strongest LFP signals in the OB (24,25).…”

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Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Gong

2011

Proc. Natl. Acad. Sci. U.S.A.

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It is critical for normal brains to perceive the external world precisely and accurately under ever-changing operational conditions, yet the mechanisms underlying this fundamental brain function in the sensory systems are poorly understood. To address this issue in the olfactory system, we investigated the responses of olfactory bulbs to odor stimulations under different brain states manipulated by anesthesia levels. Our results revealed that in two brain states, where the spontaneous baseline activities differed about twofold based on the local field potential (LFP) signals, the levels of neural activities reached after the same odor stimulation had no significant difference. This phenomenon was independent of anesthetics (pentobarbital or chloral hydrate), stimulating odorants (ethyl propionate, ethyl butyrate, ethyl valerate, amyl acetate, n-heptanal, or 2-heptanone), odor concentrations, and recording sites (the mitral or granular cell layers) for LFPs in three frequency bands and for multiunit activities. Furthermore, the activity patterns of the same stimulation under these two brain states were highly similar at both LFP and multiunit levels. These converging results argue the existence of mechanisms in the olfactory bulbs that ensure the delivery of peripheral olfactory information to higher olfactory centers with high fidelity under different brain states.T he ability to perceive the ever-changing external world accurately and precisely is a basic brain function. It is critical for daily life, survival, and higher brain functions, such as making decisions, plans, and judgments. However, the brain itself operates in ever-changing states (1, 2) or baselines (3) that are constantly modulated by external and internal factors, such as physical, physiological, psychological, clinical, and metabolic conditions. Therefore, elucidation of how sensory systems represent the same sensory information to the brain under different operational states is fundamental to understanding the related brain functions (1, 4-6).The olfactory system, as the most direct and intrinsic sensory module (1,7,8), provides a unique model to study the principles and functional mechanisms of the brain. The peripheral olfactory information takes just one synapse to enter the olfactory bulb (OB) in the brain. The OB outputs directly to the olfactory cortices that mostly belong to the limbic system. As a center to code and process the peripheral olfactory inputs and a hub to distribute the processed information to the olfactory cortices (9-11), the OB consists of laminar structures, from the outer surface to the inner core: the olfactory nerve, glomerular, external plexiform, mitral cell layer (MCL), and granular cell (GCL) layer. All peripheral olfactory input is received by a few thousand glomeruli, which generate an odor-specific spatiotemporal activity pattern across the glomerular layer (10, 12, 13). The information is mainly processed in the external plexiform layer that contains a dense dendrodendritic network formed between the secon...

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“…G amma oscillations (40-100 Hz) are produced in the mammalian olfactory bulb (OB) and many other structures in the nervous system (1)(2)(3). In the neocortex and the hippocampus, gamma oscillations are believed to depend on fast-spiking interneurons, created either by the interaction of inhibitory cells alone or as an interaction of excitatory pyramidal cells and inhibitory interneurons, such as basket cells (4,5).…”

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Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

Brea

Kay

Kopell

2009

Proc. Natl. Acad. Sci. U.S.A.

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Gamma oscillations in the olfactory bulb can be produced as an interaction of subthreshold oscillations (STOs) in the mitral cells (MCs) with inhibitory granule cells (GCs). The mechanism does not require that the GCs spike, and we work in a regime in which the MCs fire at rates lower than the fast gamma rhythm they create. The frequency of the network is that of the STOs, allowing the gamma to be modulated in amplitude with only small changes in frequency. Gamma oscillations could also be obtained with spiking GCs, but only for GCs firing close to population rate. Our mechanism differs from the more standard description of the gamma oscillation, in which the the decay time of the inhibitory cells is critical to the frequency of the network.mitral cell ͉ granule cell ͉ graded inhibition G amma oscillations (40-100 Hz) are produced in the mammalian olfactory bulb (OB) and many other structures in the nervous system (1-3). In the neocortex and the hippocampus, gamma oscillations are believed to depend on fast-spiking interneurons, created either by the interaction of inhibitory cells alone or as an interaction of excitatory pyramidal cells and inhibitory interneurons, such as basket cells (4,5). It is generally accepted that interactions between excitatory mitral cells (MCs) and inhibitory granule cells (GCs) at the dendrodendritic reciprocal synapse support gamma oscillations in the OB, but the physiological mechanisms of these oscillations are not well understood. Many slice studies focus on regimes in which the axonless GCs spike. However, it has been suggested, by contrast, that gamma oscillations in the OB depend on the subtheshold oscillations (STOs) in MCs, the excitatory cells of the OB (6), and that spikes from the GCs, the inhibitory cells of the OB, may not play a major part in the gamma oscillation of the OB (ref. 7 and see also Discussion). It is not understood what differences these features might make in the mechanism of synchronization of the OB gamma rhythm.It is well known that a target population of cells can be synchronized by a common pulse of inhibition (5,8,9). The synchronization comes mainly from a shared suppression of firing until the inhibition has worn off sufficiently for the excitatory cells to fire. If the target cells are identical in drive, they will fire simultaneously; if they have somewhat different drives, they will fire with a small lag (5). With graded inhibition, it is less clear how the inhibition provides the synchronization: there is no clear decay time of inhibition, because the amplitude and time course of the inhibition is not stereotyped.Here, we show that the features of STOs and graded inhibition can work together to produce a mechanism for the synchronization of gamma. We are interested in the regime in which MCs, the excitatory cells of the OB, spike with a firing rate significantly below that of the population frequency, as seen experimentally (10). Unlike the classical excitation-inhibition of the pyramidal interneuron network gamma (PING), in which the decay t...

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Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system

Cited by 101 publications

References 86 publications

How Global Are Olfactory Bulb Oscillations?

How Global Are Olfactory Bulb Oscillations?

Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations

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