Synchronized Oscillatory Discharges of Mitral/Tufted Cells With Different Molecular Receptive Ranges in the Rabbit Olfactory Bulb

Individual glomeruli in the mammalian olfactory bulb represent a single or a few type(s) of odorant receptors. Signals from different types of receptors are thus sorted out into different glomeruli. How does the neuronal circuit in the olfactory bulb contribute to the combination and integration of signals received by different glomeruli? Here we examined electrophysiologically whether there were functional interactions between mitral/tufted cells associated with different glomeruli in the rabbit olfactory bulb. First, we made simultaneous recordings of extracellular single-unit spike responses of mitral/tufted cells and oscillatory local field potentials in the dorsomedial fatty acid–responsive region of the olfactory bulb in urethan-anesthetized rabbits. Using periodic artificial inhalation, the olfactory epithelium was stimulated with a homologous series of n-fatty acids or n-aliphatic aldehydes. The odor-evoked spike discharges of mitral/tufted cells tended to phase-lock to the oscillatory local field potential, suggesting that spike discharges of many cells occur synchronously during odor stimulation. We then made simultaneous recordings of spike discharges from pairs of mitral/tufted cells located 300–500 μm apart and performed a cross-correlation analysis of their spike responses to odor stimulation. In ∼27% of cell pairs examined, two cells with distinct molecular receptive ranges showed synchronized oscillatory discharges when olfactory epithelium was stimulated with one or a mixture of odorant(s) effective in activating both. The results suggest that the neuronal circuit in the olfactory bulb causes synchronized spike discharges of specific pairs of mitral/tufted cells associated with different glomeruli and the synchronization of odor-evoked spike discharges may contribute to the temporal binding of signals derived from different types of odorant receptor.

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

European Journal of Neuroscience ◽

10.1111/j.1460-9568.2008.06123.x ◽

2008 ◽

Vol 27 (6) ◽

pp. 1432-1440 ◽

Cited By ~ 25

Author(s):

Tristan Cenier ◽

Corine Amat ◽

Philippe Litaudon ◽

Samuel Garcia ◽

Pierre Lafaye de Micheaux ◽

...

Keyword(s):

Olfactory Bulb ◽

Vapor Pressure ◽

Local Field ◽

Local Field Potential ◽

Field Potential

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Pharmacological manipulation of the olfactory bulb modulates beta oscillations: testing model predictions

Journal of Neurophysiology ◽

10.1152/jn.00090.2018 ◽

2018 ◽

Vol 120 (3) ◽

pp. 1090-1106 ◽

Cited By ~ 7

Author(s):

Bolesław L. Osinski ◽

Alex Kim ◽

Wenxi Xiao ◽

Nisarg M. Mehta ◽

Leslie M. Kay

Keyword(s):

Nmda Receptor ◽

Olfactory Bulb ◽

Local Field ◽

Local Field Potential ◽

Field Potential ◽

Gamma Oscillations ◽

Receptor Activation ◽

Beta Oscillations ◽

Pyriform Cortex ◽

Beta Power

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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Odorant receptor proteins in the mouse main olfactory epithelium and olfactory bulb

Neuroscience ◽

10.1016/j.neuroscience.2016.12.044 ◽

2017 ◽

Vol 344 ◽

pp. 167-177 ◽

Cited By ~ 3

Author(s):

Victoria F. Low ◽

Peter Mombaerts

Keyword(s):

Olfactory Bulb ◽

Olfactory Epithelium ◽

Odorant Receptor ◽

Receptor Proteins ◽

Main Olfactory Epithelium

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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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Coupling of tactile LFP signals between mouse cortex and olfactory bulb

10.1101/144279 ◽

2017 ◽

Author(s):

Ana Parabucki ◽

Ilan Lampl

Keyword(s):

Olfactory Bulb ◽

Local Field ◽

Orbitofrontal Cortex ◽

Barrel Cortex ◽

Brain Activity ◽

Field Potential ◽

Field Potentials ◽

Mouse Cortex ◽

Highly Correlated ◽

Potential Signal

SummaryLocal field potentials are an important measure of brain activity and have been used to address various mechanistic and behavioral questions. We revealed a prominent whisker evoked local field potential signal in the olfactory bulb and investigated its physiology. This signal, dependent on barrel cortex activation and highly correlated with its local activity, represented a pure volume conductance signal that was sourced back to the activity in the ventro-lateral orbitofrontal cortex, located a few millimeters away. Thus, we suggest that special care should be taken when acquiring and interpreting LFP data.

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Current-Source Density Analysis in the Rat Olfactory Bulb: Laminar Distribution of Kainate/AMPA- and NMDA-Receptor-Mediated Currents

Journal of Neurophysiology ◽

10.1152/jn.1999.81.1.15 ◽

1999 ◽

Vol 81 (1) ◽

pp. 15-28 ◽

Cited By ~ 37

Author(s):

Vassiliki Aroniadou-Anderjaska ◽

Matthew Ennis ◽

Michael T. Shipley

Keyword(s):

Nmda Receptor ◽

Olfactory Bulb ◽

Granule Cell ◽

Granule Cells ◽

Current Source ◽

Field Potential ◽

Current Source Density ◽

Source Density ◽

Tufted Cells ◽

Apical Dendrites

Aroniadou-Anderjaska, Vassiliki, Matthew Ennis, and Michael T. Shipley. Current-source density analysis in the rat olfactory bulb: laminar distribution of kainate/AMPA- and NMDA-receptor-mediated currents. J. Neurophysiol. 81: 15–28, 1999. The one-dimensional current-source density method was used to analyze laminar field potential profiles evoked in rat olfactory bulb slices by stimulation in the olfactory nerve (ON) layer or mitral cell layer (MCL) and to identify the field potential generators and the characteristics of synaptic activity in this network. Single pulses to the ON evoked a prolonged (≥400 ms) sink (S1ON) in the glomerular layer (GL) with corresponding sources in the external plexiform layer (EPL) and MCL and a relatively brief sink (S2ON) in the EPL, reversing in the internal plexiform and granule cell layers. These sink/source distributions suggested that S1ON and S2ON were generated in the apical dendrites of mitral/tufted cells and granule cells, respectively. The kainate/AMPA-receptor antagonist CNQX (10 μM) reduced the early phase of S1ON, blocked S2ON, and revealed a low amplitude, prolonged sink at the location of S2ON in the EPL. Reduction of Mg2+, in CNQX, enhanced both the CNQX-resistant component of S1ON and the EPL sink. This EPL sink reversed below the MCL, suggesting it was produced in granule cells. The NMDA-receptor antagonist APV (50 μM) reversibly blocked the CNQX-resistant field potentials in all layers. Single pulses were applied to the MCL to antidromically depolarize the dendrites of mitral/tufted cells. In addition to synaptic currents of granule cells, a low-amplitude, prolonged sink (S1mcl) was evoked in the GL. Corresponding sources were in the EPL, suggesting that S1mcl was generated in the glomerular dendritic tufts of mitral/tufted cells. Both S1mcl and the granule cell currents were nearly blocked by CNQX (10 μM) but enhanced by subsequent reduction of Mg2+; these currents were blocked by APV. S1mcl also was enhanced by γ-aminobutyric acid-A-receptor antagonists applied to standard medium; this enhancement was reduced by APV. ON activation produces prolonged excitation in the apical dendrites of mitral/tufted cells, via kainate/AMPA and NMDA receptors, providing the opportunity for modulation and integration of sensory information at the first level of synaptic processing in the olfactory system. Granule cells respond to input from the lateral dendrites of mitral/tufted cells via both kainate/AMPA and NMDA receptors; however, in physiological concentrations of extracellular Mg2+, NMDA-receptor activation does not contribute significantly to the granule cell responses. The glomerular sink evoked by antidromic depolarization of mitral/tufted cell dendrites suggests that glutamate released from the apical dendrites of mitral/tufted cells may excite the same or neighboring mitral/tufted cell dendrites.

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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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