scholarly journals Pharmacological manipulation of olfactory bulb granule cell excitability modulates beta oscillations: Testing a model

2017 ◽  
Author(s):  
Boleslaw L. Osinski ◽  
Alex Kim ◽  
Wenxi Xiao ◽  
Nisarg Mehta ◽  
Leslie M. Kay
Keyword(s):  
Olfactory Bulb ◽  
Granule Cell ◽  
Piriform Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
List Type ◽  
Muscarinic Agonist ◽  
Beta Oscillations ◽  
Cell Excitability ◽  
Beta Power

AbstractThe mammalian olfactory bulb (OB) generates gamma (40 – 100 Hz) and beta (15 – 30 Hz) oscillations of the local field potential (LFP). Gamma oscillations arise at the peak of inhalation supported by dendrodendritic interactions between glutamatergic mitral cells (MCs) and GABAergic granule cells (GCs). Beta oscillations occur in response to odorants in learning or odor sensitization paradigms, but their generation mechanism and function are still poorly understood. When centrifugal inputs to the OB are blocked, beta oscillations disappear, but gamma oscillations persist. Centrifugal input targets primarily GABAergic interneurons in the GC layer (GCL) and regulates GC excitability, which suggests a causal link between beta oscillations and GC excitability. Previous modeling work from our laboratory predicted that convergence of excitatory/inhibitory inputs onto MCs and centrifugal inputs onto GCs can increase GC excitability sufficiently to drive beta oscillations primarily through voltage dependent calcium channel (VDCC) mediated GABA release, independently of NMDA channels. We test this model by examining the influence of NMDA and muscarinic acetylcholine receptors on GC excitability and beta oscillations. Intrabulbar scopolamine (muscarinic antagonist) infusion decreased or completely 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. Piriform cortex (PC) beta power was unchanged. Oxotremorine (muscarinic agonist) tended to suppress all oscillations, probably from over-inhibition. 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 by VDCC mediated currents.New and Noteworthy:Olfactory bulb beta oscillations rely on granule cell excitability.Reducing granule cell excitability with scopolamine reduces high volatilityinduced beta power but increases low volatility-induced beta power.Piriform cortex beta oscillations maintain power when olfactory bulb beta power is low, and the system maintains beta band coherence.

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

2018 ◽  
Vol 120 (3) ◽  
pp. 1090-1106 ◽  
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.

Chemical Factors Determine Olfactory System Beta Oscillations in Waking Rats

2007 ◽  
Vol 98 (1) ◽  
pp. 394-404 ◽  
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.

scholarly journals Granule cell excitability regulates gamma and beta oscillations in a model of the olfactory bulb dendrodendritic microcircuit

2016 ◽  
Vol 116 (2) ◽  
pp. 522-539 ◽  
Author(s):  
Bolesław L. Osinski ◽  
Leslie M. Kay
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Causal Link ◽  
Beta Oscillations ◽  
Gamma Frequency ◽  
Voltage Dependent ◽  
Nmda Channels ◽  
Beta Frequency

Odors evoke gamma (40–100 Hz) and beta (20–30 Hz) oscillations in the local field potential (LFP) of the mammalian olfactory bulb (OB). Gamma (and possibly beta) oscillations arise from interactions in the dendrodendritic microcircuit between excitatory mitral cells (MCs) and inhibitory granule cells (GCs). When cortical descending inputs to the OB are blocked, beta oscillations are extinguished whereas gamma oscillations become larger. Much of this centrifugal input targets inhibitory interneurons in the GC layer and regulates the excitability of GCs, which suggests a causal link between the emergence of beta oscillations and GC excitability. We investigate the effect that GC excitability has on network oscillations in a computational model of the MC-GC dendrodendritic network with Ca2+-dependent graded inhibition. Results from our model suggest that when GC excitability is low, the graded inhibitory current mediated by NMDA channels and voltage-dependent Ca2+ channels (VDCCs) is also low, allowing MC populations to fire in the gamma frequency range. When GC excitability is increased, the activation of NMDA receptors and other VDCCs is also increased, allowing the slow decay time constants of these channels to sustain beta-frequency oscillations. Our model argues that Ca2+ flow through VDCCs alone could sustain beta oscillations and that the switch between gamma and beta oscillations can be triggered by an increase in the excitability state of a subpopulation of GCs.

scholarly journals Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

2019 ◽  
Author(s):  
Justin Losacco ◽  
Daniel Ramirez-Gordillo ◽  
Jesse Gilmer ◽  
Diego Restrepo
Keyword(s):  
Olfactory Bulb ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Brain Regions ◽  
Spike Timing ◽  
Potential Oscillations ◽  
Theta Oscillation ◽  
Beta Power ◽  
Early Processing ◽  
Theta Phase

AbstractLocal field potential oscillations reflect temporally coordinated neuronal ensembles— coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.SignificanceEarly processing of olfactory information takes place in circuits undergoing slow frequency theta oscillations generated by the interplay of olfactory input modulated by sniffing and centrifugal feedback from downstream brain areas. Studies in the hippocampus and cortex suggest that different information “chunks” are conveyed at different phases of the theta oscillation. Here we show that in the olfactory bulb, the first processing station in the olfactory system, the amplitude of high frequency gamma oscillations encodes for information on whether an odorant is rewarded when it is observed at the peak phase of the theta oscillation. Furthermore, encoding of information by the theta phase-referenced gamma oscillations becomes more accurate as the animal learns to differentiate two odorants.

scholarly journals A Beta Oscillation Network in the Rat Olfactory System During a 2-Alternative Choice Odor Discrimination Task

2010 ◽  
Vol 104 (2) ◽  
pp. 829-839 ◽  
Author(s):  
Leslie M. Kay ◽  
Jennifer Beshel
Keyword(s):  
Frequency Band ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Beta Band ◽  
Beta Oscillations ◽  
Odor Discrimination Task ◽  
Beta Power ◽  
Beta Frequency Band ◽  
Alternative Choice ◽  
Beta Frequency

We previously showed that in a two-alternative choice (2AC) task, olfactory bulb (OB) gamma oscillations (∼70 Hz in rats) were enhanced during discrimination of structurally similar odorants (fine discrimination) versus discrimination of dissimilar odorants (coarse discrimination). In other studies (mostly employing go/no-go tasks) in multiple labs, beta oscillations (15–35 Hz) dominate the local field potential (LFP) signal in olfactory areas during odor sampling. Here we analyzed the beta frequency band power and pairwise coherence in the 2AC task. We show that in a task dominated by gamma in the OB, beta oscillations are also present in three interconnected olfactory areas (OB and anterior and posterior pyriform cortex). Only the beta band showed consistently elevated coherence during odor sniffing across all odor pairs, classes (alcohols and ketones), and discrimination types (fine and coarse), with stronger effects in first than in final criterion sessions (>70% correct). In the first sessions for fine discrimination odor pairs, beta power for incorrect trials was the same as that for correct trials for the other odor in the pair. This pattern was not repeated in coarse discrimination, in which beta power was elevated for correct relative to incorrect trials. This difference between fine and coarse odor discriminations may relate to different behavioral strategies for learning to differentiate similar versus dissimilar odors. Phase analysis showed that the OB led both pyriform areas in the beta frequency band during odor sniffing. We conclude that the beta band may be the means by which information is transmitted from the OB to higher order areas, even though task specifics modify dominance of one frequency band over another within the OB.

scholarly journals Network and synaptic mechanisms underlying high frequency oscillations in the rat and cat olfactory bulb under ketamine-xylazine anesthesia

2020 ◽  
Author(s):  
Władysław Średniawa ◽  
Jacek Wróbel ◽  
Ewa Kublik ◽  
Daniel Krzysztof Wójcik ◽  
Miles Adrian Whittington ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
High Frequency ◽  
Piriform Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Synaptic Activity ◽  
Surgical Removal ◽  
Nasal Airflow ◽  
High Frequency Oscillations ◽  
Subcortical Regions

AbstractHigh frequency oscillations (HFO) are receiving increased attention for their role in health and disease. Ketamine-dependent HFO have been identified in cortical and subcortical regions in rodents, however, the mechanisms underlying their generation and whether they occur in higher mammals is unclear. Here, we show under ketamine-xylazine anesthesia, classical gamma oscillations diminish and a prominent > 80 Hz oscillation emerges in the olfactory bulb of rats and cats. In cats negligible HFO was observed in the thamalus and visual cortex indicating the OB was a suitable site for further investigation. Simultaneous local field potential and thermocouple recordings demonstrated HFO was dependent on nasal airflow. Silicon probe mapping studies spanning almost the entire dorsal ventral aspect of the OB revealed this rhythm was strongest in ventral areas of the bulb and associated with microcurrent sources about the mitral layer. Pharmacological microinfusion studies revealed HFO was dependent on excitatory-inhibitory synaptic activity, but not gap junctions. Finally, we showed HFO was preserved despite surgical removal of the piriform cortex. We conclude that ketamine-dependent HFO in the OB are driven by nasal airflow and local dendrodendritic interactions. The relevance of our findings to ketamine’s model of psychosis in awake state are also discussed.

scholarly journals Enhanced LTP of population spikes in the dentate gyrus of mice haploinsufficient for neurobeachin

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Julia Muellerleile ◽  
Aline Blistein ◽  
Astrid Rohlmann ◽  
Frederieke Scheiwe ◽  
Markus Missler ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Granule Cell ◽  
Field Potential ◽  
Synaptic Function ◽  
Spatial Learning And Memory ◽  
Neurotransmitter Receptor ◽  
Cell Excitability ◽  
Neuronal Protein ◽  
Electrophysiological Recordings

Abstract Deletion of the autism candidate molecule neurobeachin (Nbea), a large PH-BEACH-domain containing neuronal protein, has been shown to affect synaptic function by interfering with neurotransmitter receptor targeting and dendritic spine formation. Previous analysis of mice lacking one allele of the Nbea gene identified impaired spatial learning and memory in addition to altered autism-related behaviours. However, no functional data from living heterozygous Nbea mice (Nbea+/−) are available to corroborate the behavioural phenotype. Here, we explored the consequences of Nbea haploinsufficiency on excitation/inhibition balance and synaptic plasticity in the intact hippocampal dentate gyrus of Nbea+/− animals in vivo by electrophysiological recordings. Based on field potential recordings, we show that Nbea+/− mice display enhanced LTP of the granule cell population spike, but no differences in basal synaptic transmission, synapse numbers, short-term plasticity, or network inhibition. These data indicate that Nbea haploinsufficiency causes remarkably specific alterations to granule cell excitability in vivo, which may contribute to the behavioural abnormalities in Nbea+/− mice and to related symptoms in patients.

scholarly journals Gamma oscillations in the rat ventral striatum originate in the piriform cortex

2017 ◽  
Author(s):  
James E. Carmichael ◽  
Jimmie M. Gmaz ◽  
Matthijs A. A. van der Meer
Keyword(s):  
Local Field ◽  
Ventral Striatum ◽  
Piriform Cortex ◽  
Current Source ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Gamma Band ◽  
Temporal Organization ◽  
Local Circuitry ◽  
Gamma Band Oscillations

AbstractLocal field potentials (LFP) recorded from the human and rodent ventral striatum (vStr) exhibit prominent, behaviorally relevant gamma-band oscillations. These oscillations are related to local spiking activity and transiently synchronize with anatomically related areas, suggesting a possible role in organizing vStr activity. However, the origin of vStr gamma is unknown. We recorded vStr gamma oscillations across a 1.4mm2 grid spanned by 64 recording electrodes as rats rested and foraged for rewards, revealing a highly consistent power gradient originating in the adjacent piriform cortex. Phase differences across the vStr were consistently small (<10°) and current source density analysis further confirmed the absence of local sink-source pairs in the vStr. Reversible occlusions of the ipsilateral (but not contralateral) nostril, known to abolish gamma oscillations in the piriform cortex, strongly reduced vStr gamma power and the occurrence of transient gamma-band events. These results imply that local circuitry is not a major contributor to gamma oscillations in the vStr LFP, and that piriform cortex is an important driver of gamma-band oscillations in the vStr and associated limbic areas.Significance StatementThe ventral striatum is an area of anatomical convergence in circuits underlying motivated behavior, but it remains unclear how its inputs from different sources interact. One of the major proposals of how neural circuits may dynamically switch between convergent inputs is through temporal organization reflected in local field potential (LFP) oscillations. Our results show that in the rat, the mechanisms controlling vStr gamma oscillations are primarily located in the in the adjacent piriform cortex, rather than vStr itself. This provides a novel interpretation of previous rodent work on gamma oscillations in the vStr and related circuits, and an important consideration for future work seeking to use oscillations in these areas as biomarkers in rodent models of human behavioral and neurological disorders.

scholarly journals Perturbation of in vivo neural activity following α-Synuclein seeding in the olfactory bulb

2020 ◽  
Author(s):  
Aishwarya S. Kulkarni ◽  
Maria del Mar Cortijo ◽  
Elizabeth R. Roberts ◽  
Tamara L. Suggs ◽  
Heather B. Stover ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Neural Activity ◽  
Olfactory System ◽  
Piriform Cortex ◽  
Field Potential ◽  
Dopamine Neurons ◽  
Motor Deficits ◽  
Wild Type ◽  
Evoked Activity

AbstractBACKGROUNDParkinson’s disease (PD) neuropathology is characterized by intraneuronal protein aggregates composed of misfolded α-Synuclein (α-Syn), as well as degeneration of substantia nigra dopamine neurons. Deficits in olfactory perception and aggregation of α-Syn in the olfactory bulb (OB) are observed during early stages of PD, and have been associated with the PD prodrome, before onset of the classic motor deficits. α-Syn fibrils injected into the OB of mice cause progressive propagation of α-Syn pathology throughout the olfactory system and are coupled to olfactory perceptual deficits.OBJECTIVEWe hypothesized that accumulation of pathogenic α-Syn in the OB impairs neural activity in the olfactory system.METHODSTo address this, we monitored spontaneous and odor-evoked local field potential dynamics in awake wild type mice simultaneously in the OB and piriform cortex (PCX) one, two, and three months following injection of pathogenic preformed α-Syn fibrils in the OB.RESULTSWe detected α-Syn pathology in both the OB and PCX. We also observed that α-Syn fibril injections influenced odor-evoked activity in the OB. In particular, α-Syn fibril-injected mice displayed aberrantly high odor-evoked power in the beta spectral range. A similar change in activity was not detected in the PCX, despite high levels of α-Syn pathology.CONCLUSIONSTogether, this work provides evidence that synucleinopathy impacts in vivo neural activity in the olfactory system at the network-level.

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