Beta and Gamma Oscillations in the Olfactory System of the Urethane-Anesthetized Rat

Neville, Kevin R.; Haberly, Lewis B.

doi:10.1152/jn.00475.2003

Cited by 275 publications

(293 citation statements)

References 43 publications

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“…Recently, a current source density analysis revealed that the granule cell dipoles provide large current flows during ␥ oscillations (Neville and Haberly, 2003). In line with this, we found that the major part of the currents leading to LFP oscillations came from the EPL, near the MCL, with an inversion below the MCL (Fig.…”

Section: Nature Of Field ␥ Oscillationssupporting

confidence: 85%

“…Previous theoretical investigations have suggested that granule cells, the largest population of bulbar interneurons, constitute the main generators of extracellular current flows (Rall and Shepherd, 1968;Freeman, 1975), but in vivo data supporting this assumption came out only recently (Neville and Haberly, 2003). The relative contribution of granule cells and bulbar output neurons (i.e., mitral/tufted cells) implicated in fast oscillations still remains speculative, although a phase relationship between mitral/tufted cell spiking activity and LFP oscillations has been found (Kashiwadani et al, 1999;Buonviso et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…In addition, although clearly ␥ oscillations originate from intrinsic bulbar circuitry because they are abolished in the piriform cortex by OB removal (Becker and Freeman, 1968) and preserved when conduction through the olfactory peduncle is blocked (Gray and Skinner, 1988;Neville and Haberly, 2003), the cellular mechanisms responsible for their maintenance are still unknown. Previous analysis of LFP oscillations suggested distinct mechanisms including: (1) a fast synaptic inhibitory feedback loop between mitral/tufted cells and granule cells (Mori and Takagi, 1977;Gray and Skinner, 1988;Eeckman and Freeman, 1990;Nusser et al, 2001;Friedman and Strowbridge, 2003); (2) intrinsic membrane properties of mitral/tufted cells (Desmaisons et al, 1999); (3) odorant-induced sensory neuron oscillations (Nikonov et al, 2002); and (4) electrical couplings between interneurons (Friedman and Strowbridge, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

Lagier¹,

Carleton²,

Lledo³

2004

J. Neurosci.

241

223

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Olfactory stimuli have been known for a long time to elicit oscillations in olfactory brain areas. In the olfactory bulb (OB), odors trigger synchronous oscillatory activity that is believed to arise from the coherent and rhythmic discharges of large numbers of neurons. These oscillations are known to take part in encoding of sensory information before their transfer to higher subcortical and cortical areas. To characterize the cellular mechanisms underlying ␥ (30 -80 Hz) local field potential (LFP) oscillations, we simultaneously recorded multiunit discharges, intracellular responses, and LFP in rat OB slices. We showed that a single and brief electrical stimulation of olfactory nerve elicited LFP oscillations in the mitral cell body layer lasting Ͼ1 sec. Both action potentials and subthreshold oscillations of mitral/tufted cells, the bulbar output neurons, were precisely synchronized with LFP oscillations. This synchronization arises from the interaction between output neurons and granule cells, the main population of local circuit inhibitory interneurons, through dendrodendritic synapses. Interestingly enough, the synchronization exerted by reciprocal synaptic interactions did not require action potentials initiated in granule cell somata. Finally, local application of a GABA A receptor antagonist at the mitral cell and external plexiform layers confirmed the exclusive role of the granule cell reciprocal synapses in generating the evoked oscillations. We concluded that interneurons located in the granule cell layer generate synaptic activity capable of synchronizing activity of output neurons by interacting with both their subthreshold and spiking activity.

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Section: Nature Of Field ␥ Oscillationssupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

Lagier¹,

Carleton²,

Lledo³

2004

J. Neurosci.

241

223

View full text Add to dashboard Cite

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“…We also measured the local field potential (LFP) from the mitral cell layer, which allowed us to record subthreshold activity from both mitral and granule cells (39). At rest, with the nostril open, breathing induced theta-frequency deflections, and odors elicited gamma oscillations (Fig.…”

Section: S2dmentioning

confidence: 99%

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Patterson

Lagier

Carleton

2013

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

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Rodents can discriminate odors in one breath, and mammalian olfaction research has thus focused on the first breath. However, sensory representations dynamically change during and after stimuli. To investigate these dynamics, we recorded spike trains from the olfactory bulb of awake, head-fixed mice and found that some mitral cells' odor representations changed following the first breath and others continued after odor cessation. Population analysis revealed that these postodor responses contained odor-and concentration-specific information-an odor afterimage. Using calcium imaging, we found that most olfactory glomerular activity was restricted to the odor presentation, implying that the afterimage is not primarily peripheral. The odor afterimage was not dependent on odorant physicochemical properties. To artificially induce aftereffects, we photostimulated mitral cells using channelrhodopsin and recorded centrally maintained persistent activity. The strength and persistence of the afterimage was dependent on the duration of both artificial and natural stimulation. In summary, we show that the odor representation evolves after the first breath and that there is a centrally maintained odor afterimage, similar to other sensory systems. These dynamics may help identify novel odorants in complex environments.multielectrode recording | network dynamics | optogenetics S ensory systems, even when presented with fixed stimuli, use dynamic neural representations that change over time. These changes range from simple potentiation or adaptation to more complex temporal patterns (1, 2). These dynamics can persist even after the cessation of stimulus, which can take the form of an off-response or prolonged aftereffect. Aftereffects have been intensely studied in vision (1, 3) and also observed in audition (4, 5), touch (6, 7), taste (here the afterimages may be due to persistent ligand binding) (8, 9), and insect olfaction (10, 11). In mammalian olfaction, the only reported aftereffect is a "persistent afterdischarge" following high concentration odors (12).Olfaction is an active process that is coordinated by breathing (2, 13). Odorants bind to odorant receptor neurons (ORNs) in the epithelium, which synapse onto mitral/tufted (M/T) cells in the olfactory bulb (OB) at precisely defined glomeruli. Direct recordings of ORNs in rats show that ORNs are excited by odors and that activity can last for seconds after odor cessation (14). Others have measured the output of ORNs, by imaging glomeruli, and found that the response is gated by each breath and that the amplitude decreases with time (13, 15). The importance of breath segmentation for M/T cells has recently been shown in awake subjects, where neurons respond with precise, phasic firing patterns (16-18). However, these recordings have focused on how information is represented during the first breath, as rodents can identify odors in a single breath (19)(20)(21). Activity in piriform cortex is also segmented by breaths, and neurons there respond sparsely (22,23), and with a...

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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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confidence: 99%

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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Beta and Gamma Oscillations in the Olfactory System of the Urethane-Anesthetized Rat

Cited by 275 publications

References 43 publications

Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

Interplay between Local GABAergic Interneurons and Relay Neurons Generates γ Oscillations in the Rat Olfactory Bulb

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

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

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