Odor vapor pressure and quality modulate local field potential oscillatory patterns in the olfactory bulb of the anesthetized rat

The mammalian olfactory bulb (OB) generates gamma (40–100 Hz) and beta (15–30 Hz) local field potential (LFP) oscillations. Gamma oscillations arise at the peak of inhalation supported by dendrodendritic interactions between glutamatergic mitral cells (MCs) and GABAergic granule cells (GCs). Beta oscillations are induced by odorants in learning or odor sensitization paradigms, but their mechanism and function are still poorly understood. When centrifugal OB inputs are blocked, beta oscillations disappear, but gamma oscillations persist. Centrifugal inputs target primarily GABAergic interneurons in the GC layer (GCL) and regulate GC excitability, suggesting a causal link between beta oscillations and GC excitability. Our previous modeling work predicted that convergence of excitatory/inhibitory inputs onto MCs and centrifugal inputs onto GCs increase GC excitability sufficiently to produce beta oscillations primarily through voltage dependent calcium channel-mediated GABA release, independently of NMDA channels. We test some of the predictions of this model by examining the influence of NMDA and muscarinic acetylcholine (ACh) receptors, which affect GC excitability in different ways, on beta oscillations. A few minutes after intrabulbar infusion, scopolamine (muscarinic antagonist) suppressed odor-evoked beta in response to a strong stimulus but increased beta power in response to a weak stimulus, as predicted by our model. Pyriform cortex (PC) beta power was unchanged. Oxotremorine (muscarinic agonist) suppressed all oscillations, likely from overinhibition. APV, an NMDA receptor antagonist, suppressed gamma oscillations selectively (in OB and PC), lending support to the model’s prediction that beta oscillations can be supported independently of NMDA receptors. NEW & NOTEWORTHY Olfactory bulb local field potential beta oscillations appear to be gated by GABAergic granule cell excitability. Reducing excitability with scopolamine reduces beta induced by strong odors but increases beta induced by weak odors. Beta oscillations rely on the same synapse as gamma oscillations but, unlike gamma, can persist in the absence of NMDA receptor activation. Pyriform cortex beta oscillations maintain power when olfactory bulb beta power is low, and the system maintains beta band coherence.

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Chemical Factors Determine Olfactory System Beta Oscillations in Waking Rats

Journal of Neurophysiology ◽

10.1152/jn.00124.2007 ◽

2007 ◽

Vol 98 (1) ◽

pp. 394-404 ◽

Cited By ~ 47

Author(s):

Catherine A. Lowry ◽

Leslie M. Kay

Keyword(s):

Olfactory Bulb ◽

Vapor Pressure ◽

Vapor Phase ◽

Local Field ◽

Olfactory System ◽

Piriform Cortex ◽

Field Potential ◽

Gamma Oscillations ◽

Beta Oscillations ◽

Phase Concentration

Recent studies have pointed to olfactory system beta oscillations of the local field potential (15–30 Hz) and their roles both in learning and as specific responses to predator odors. To describe odorant physical properties, resultant behavioral responses and changes in the central olfactory system that may induce these oscillations without associative learning, we tested rats with 26 monomolecular odorants spanning 6 log units of theoretical vapor pressure (estimate of relative vapor phase concentration) and 10 different odor mixtures. We found odorant vapor phase concentration to be inversely correlated with investigation time on the first presentation, after which investigation times were brief and not different across odorants. Analysis of local field potentials from the olfactory bulb and anterior piriform cortex shows that beta oscillations in waking rats occur specifically in response to the class of volatile organic compounds with vapor pressures of 1–120 mmHg. Beta oscillations develop over the first three to four presentations and are weakly present for some odorants in anesthetized rats. Gamma oscillations show a smaller effect that is not restricted to the same range of odorants. Olfactory bulb theta oscillations were also examined as a measure of effective afferent input strength, and the power of these oscillations did not vary systematically with vapor pressure, suggesting that it is not olfactory bulb drive strength that determines the presence of beta oscillations. Theta band coherence analysis shows that coupling strength between the olfactory bulb and piriform cortex increases linearly with vapor phase concentration, which may facilitate beta oscillations above a threshold.

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How Global Are Olfactory Bulb Oscillations?

Journal of Neurophysiology ◽

10.1152/jn.00478.2010 ◽

2010 ◽

Vol 104 (3) ◽

pp. 1768-1773 ◽

Cited By ~ 20

Author(s):

Leslie M. Kay ◽

Philip Lazzara

Keyword(s):

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Field Potential ◽

Beta Band ◽

Recording Site ◽

Potential Oscillations ◽

Frequency Bands ◽

Surface Electrodes ◽

Analysis Window

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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In vivo beta and gamma subthreshold oscillations in rat mitral cells: origin and gating by respiratory dynamics

Journal of Neurophysiology ◽

10.1152/jn.00053.2017 ◽

2018 ◽

Vol 119 (1) ◽

pp. 274-289 ◽

Cited By ~ 1

Author(s):

Nicolas Fourcaud-Trocmé ◽

Virginie Briffaud ◽

Marc Thévenet ◽

Nathalie Buonviso ◽

Corine Amat

Keyword(s):

Membrane Potential ◽

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Respiratory Rhythm ◽

Field Potential ◽

Synaptic Activity ◽

Spike Discharge ◽

Subthreshold Oscillations

In mammals, olfactory bulb (OB) dynamics are paced by slow and fast oscillatory rhythms at multiple levels: local field potential, spike discharge, and/or membrane potential oscillations. Interactions between these levels have been well studied for the slow rhythm linked to animal respiration. However, less is known regarding rhythms in the fast beta (10–35 Hz) and gamma (35–100 Hz) frequency ranges, particularly at the membrane potential level. Using a combination of intracellular and extracellular recordings in the OB of freely breathing rats, we show that beta and gamma subthreshold oscillations (STOs) coexist intracellularly and are related to extracellular local field potential (LFP) oscillations in the same frequency range. However, they are differentially affected by changes in cell excitability and by odor stimulation. This leads us to suggest that beta and gamma STOs may rely on distinct mechanisms: gamma STOs would mainly depend on mitral cell intrinsic resonance, while beta STOs could be mainly driven by synaptic activity. In a second study, we find that STO occurrence and timing are constrained by the influence of the slow respiratory rhythm on mitral and tufted cells. First, respiratory-driven excitation seems to favor gamma STOs, while respiratory-driven inhibition favors beta STOs. Second, the respiratory rhythm is needed at the subthreshold level to lock gamma and beta STOs in similar phases as their LFP counterparts and to favor the correlation between STO frequency and spike discharge. Overall, this study helps us to understand how the interaction between slow and fast rhythms at all levels of OB dynamics shapes its functional output. NEW & NOTEWORTHY In the mammalian olfactory bulb of a freely breathing anesthetized rat, we show that both beta and gamma membrane potential fast oscillation ranges exist in the same mitral and tufted (M/T) cell. Importantly, our results suggest they have different origins and that their interaction with the slow subthreshold oscillation (respiratory rhythm) is a key mechanism to organize their dynamics, favoring their functional implication in olfactory bulb information processing.

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Characterization of in utero valproic acid mouse model of autism by local field potential in the hippocampus and the olfactory bulb

Neuroscience Research ◽

10.1016/j.neures.2015.04.006 ◽

2015 ◽

Vol 98 ◽

pp. 28-34 ◽

Cited By ~ 13

Author(s):

Dania Cheaha ◽

Sara Bumrungsri ◽

Surapong Chatpun ◽

Ekkasit Kumarnsit

Keyword(s):

Valproic Acid ◽

Mouse Model ◽

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Field Potential ◽

In Utero

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Odorant modulation of neuronal activity and local field potential in sensory-deprived olfactory bulb

Neuroscience ◽

10.1016/j.neuroscience.2009.05.051 ◽

2009 ◽

Vol 162 (4) ◽

pp. 1265-1278 ◽

Cited By ~ 12

Author(s):

M.L. Aylwin ◽

G.A. Aguilar ◽

F.J. Flores ◽

P.E. Maldonado

Keyword(s):

Olfactory Bulb ◽

Neuronal Activity ◽

Local Field ◽

Local Field Potential ◽

Field Potential

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Effect of Xylazine–Tiletamine–Zolazepam on the Local Field Potential of the Rat Olfactory Bulb

Comparative Medicine ◽

10.30802/aalas-cm-20-990015 ◽

2020 ◽

Vol 70 (6) ◽

pp. 492-498

Author(s):

Peter Olegovich Kosenko ◽

Aleksey Borisovich Smolikov ◽

Viktor Borisovich Voynov ◽

Pavel Dmitrievich Shaposhnikov ◽

Anton Igorevich Saevskiy ◽

...

Keyword(s):

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Chloral Hydrate ◽

Field Potential ◽

Extended Period ◽

Information Analysis ◽

Dynamic Changes ◽

Local Field Potential Lfp ◽

Oscillatory Processes

Neural oscillations of the mammalian olfactory system have been studied for decades. This research suggests they are linked to various processes involved in odor information analysis, depending on the vigilance state and presentation of stimuli. In addition, the effects of various anesthetics, including commonly used ones like chloral hydrate, pentobarbital, ketamine, and urethane, on the local field potential (LFP) in the olfactory bulb (OB) have been studied. In particular, the combination of xylazine and tiletamine–zolazepam has been shown to produce steady anesthesia for an extended period and relatively few adverse effects; however, their effects on the LFP in the OB remain unknown. To study those effects, we recorded the LFP in the OB of rats under xylazine–tiletamine–zolazepam anesthesia. During the period of anesthesia, the spectral powers of the 1–4, 9–16, 31–64, 65–90 frequency bands increased significantly, and that of 91–170 Hz frequency band decreased significantly, whereas no significant changes were observed in the 5–8 and 17–30 Hz ranges. These results reveal dynamic changes in the time and frequency characteristics of the LFP in the OB of rats under xylazine–tiletamine– zolazepam anesthesia and suggest that this combination of anesthetics could be used for studying oscillatory processes in the OB of rats.

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Anesthetic regimes modulate the temporal dynamics of local field potential in the mouse olfactory bulb

Journal of Neurophysiology ◽

10.1152/jn.00261.2013 ◽

2014 ◽

Vol 111 (5) ◽

pp. 908-917 ◽

Cited By ~ 18

Author(s):

Romain Chery ◽

Hirac Gurden ◽

Claire Martin

Keyword(s):

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Adrenergic Receptors ◽

Temporal Dynamics ◽

Field Potential ◽

Gamma Oscillations ◽

Cell Recording ◽

The Impact ◽

Awake Condition

Anesthetized preparations have been widely used to study odor-induced temporal dynamics in the olfactory bulb. Although numerous recent data of single-cell recording or imaging in the olfactory bulb have employed ketamine cocktails, their effects on networks activities are still poorly understood, and odor-induced oscillations of the local field potential have not been characterized under these anesthetics. Our study aimed at describing the impact of two ketamine cocktails on oscillations and comparing them to awake condition. Anesthesia was induced by injection of a cocktail of ketamine, an antagonist of the N-methyl-d-aspartate receptors, combined with one agonist of α2-adrenergic receptors, xylazine (low affinity) or medetomidine (high affinity). Spontaneous and odor-induced activities were examined in anesthetized and awake conditions, in the same mice chronically implanted with an electrode in the main olfactory bulb. The overall dynamic pattern of oscillations under the two ketamine cocktails resembles that of the awake state. Ongoing activity is characterized by gamma bursts (>60 Hz) locked on respiration and beta (15–40 Hz) power increases during odor stimulation. However, anesthesia decreases local field potential power and leads to a strong frequency shift of gamma oscillations from 60–90 Hz to 100–130 Hz. We conclude that similarities between oscillations in anesthetized and awake states make cocktails of ketamine with one α2-agonist suitable for the recordings of local field potential to study processing in the early stages of the olfactory system.

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