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 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 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.

Long-Term Enhancement of Synchronized Oscillations by Adrenergic Receptor Activation in the Olfactory Bulb

2008 ◽  
Vol 99 (4) ◽  
pp. 2021-2025 ◽  
Author(s):  
David H. Gire ◽  
Nathan E. Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Associative Learning ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Olfactory Nerve ◽  
Receptor Activation ◽  
Cell Network ◽  
Functional Perspective ◽  
Gamma Frequency

The noradrenergic system is widely thought to be important for associative learning in the olfactory system through actions in the first processing structure, the main olfactory bulb (MOB). Here, we used extracellular local field potential (LFP) and patch-clamp recordings in rat MOB slices to examine norepinephrine (NE)-induced long-term changes in circuit properties that might underlie learning. During responses to patterned olfactory nerve stimulation mimicking the breathing cycle, NE induced a long-term increase in gamma frequency (30–70 Hz) synchronized oscillations. The enhancement persisted long after washout of NE (≤70 min), depended on the combined actions of NE and neuronal stimulation, and seemed to be caused by enhanced excitatory drive on the mitral/granule cell network that underlies rapid gamma oscillations. The last effect, increased excitation, was manifested as an increase in evoked long-lasting depolarizations (LLDs) in mitral cells. From a functional perspective, the observed long-term cellular and network changes could promote associative learning by amplifying odor-specific signals.

scholarly journals Age-dependent adrenergic actions in the main olfactory bulb that could underlie an olfactory-sensitive period

2012 ◽  
Vol 108 (7) ◽  
pp. 1999-2007 ◽  
Author(s):  
Sruthi Pandipati ◽  
Nathan E. Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Neural Plasticity ◽  
Granule Cells ◽  
Gamma Oscillations ◽  
Sensitive Period ◽  
Loss Of Function ◽  
Main Olfactory Bulb ◽  
Cellular Mechanisms ◽  
Gamma Frequency ◽  
Age Dependent

Many sensory systems are endowed with mechanisms of neural plasticity that are restricted to a sensitive period in the young developing animal. In this study, we performed experiments in slices of the main olfactory bulb (OB) from rats to examine possible age-dependent cellular mechanisms of plasticity in the olfactory system. We focused on the neurotransmitter norepinephrine (NE), shown to be important in different forms of olfactory learning, examining whether two specific cellular effects of NE previously observed in rats less than P14 extended to older animals. These included an acute reduction in GABAergic synaptic transmission from granule cells (GCs) onto output mitral cells (MCs) and an enhancement in gamma frequency (30–70 Hz) oscillations that persists long after removal of NE. We found that NE failed to reduce GC-to-MC transmission or enhance gamma oscillations in older rats at P18–23. The loss of NE actions on both phenomena appeared to reflect an age-dependent loss of function of α2-adrenergic receptors. In addition, we found that NE induced an age-dependent enhancement of transient excitation in MCs, providing a mechanism to link the acute decrease in GC-to-MC inhibition to the long-term increase in gamma oscillations through increases in intracellular calcium. The age-dependent cellular mechanisms that we describe could underlie an olfactory-sensitive period in newborn rodents.

scholarly journals Adrenergic Receptor-Mediated Disinhibition of Mitral Cells Triggers Long-Term Enhancement of Synchronized Oscillations in the Olfactory Bulb

2010 ◽  
Vol 104 (2) ◽  
pp. 665-674 ◽  
Author(s):  
Sruthi Pandipati ◽  
David H. Gire ◽  
Nathan E. Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Gamma Oscillations ◽  
Olfactory Learning ◽  
Inhibitory Synapses ◽  
Mitral Cells ◽  
Acute Effects ◽  
Long Term Effects ◽  
Gamma Frequency

Norepinephrine (NE) is widely implicated in various forms of associative olfactory learning in rodents, including early learning preference in neonates. Here we used patch-clamp recordings in rat olfactory bulb slices to assess cellular actions of NE, examining both acute, short-term effects of NE as well as the relationship between these acute effects and long-term cellular changes that could underlie learning. Our focus for long-term effects was on synchronized gamma frequency (30–70 Hz) oscillations, shown in prior studies to be enhanced for up to an hour after brief exposure of a bulb slice to NE and neuronal stimulation. In terms of acute effects, we found that a dominant action of NE was to reduce inhibitory GABAergic transmission from granule cells (GCs) to output mitral cells (MCs). This disinhibition was also induced by clonidine, an agonist specific for α2 adrenergic receptors (ARs). Acute NE-induced disinhibition of MCs appeared to be linked to long-term enhancement of gamma oscillations, based, first, on the fact that clonidine, but not agonists specific for other AR subtypes, mimicked NE's long-term actions. In addition, the α2 AR-specific antagonist yohimbine blocked the long-term enhancement of the oscillations due to NE. Last, brief exposure of the slice to the GABAA receptor antagonist gabazine, to block inhibitory synapses directly, also induced the long-term changes. Acute disinhibition is a plausible permissive effect of NE leading to olfactory learning, because, when combined with exposure to a specific odor, it should lead to neuron-specific increases in intracellular calcium of the type generally associated with long-term synaptic modifications.

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 Directional Coupling From the Olfactory Bulb to the Hippocampus During a Go/No-Go Odor Discrimination Task

2010 ◽  
Vol 103 (5) ◽  
pp. 2633-2641 ◽  
Author(s):  
Boris Gourévitch ◽  
Leslie M. Kay ◽  
Claire Martin
Keyword(s):  
Olfactory Bulb ◽  
Cognitive Processing ◽  
Information Transfer ◽  
Field Potential ◽  
Ventral Hippocampus ◽  
Beta Oscillations ◽  
Odor Processing ◽  
Odor Discrimination Task ◽  
Beta Frequency Band ◽  
Beta Frequency

The hippocampus and olfactory regions are anatomically close, and both play a major role in memory formation. However, the way they interact during odor processing is still unclear. In both areas, strong oscillations of the local field potential (LFP) can be recorded, and are modulated by behavior. In particular, in the olfactory system, the beta rhythm (15–35 Hz) is associated with cognitive processing of an olfactory stimulus. Using LFP recordings in the olfactory bulb and dorsal and ventral hippocampus during performance of an olfactory go/no-go task in rats, we previously showed that beta oscillations are also present in the hippocampus, coherent with those in the olfactory bulb, during odor sampling. In this study, we provide further insight into information transfer in the olfacto-hippocampal network by using directional coherence (DCOH estimate), a method based on the temporal relation between two or more signals in the frequency domain. In the theta band (6–12 Hz), coherence between the olfactory bulb (OB) and the hippocampus (HPC) is weak and can be both in the feedback and feedforward directions. However, at this frequency, modulation of the coupling between the dorsal and ventral hippocampus is seen during stimulus expectation versus odor processing. In the beta frequency band (15–35 Hz), analysis showed a strong unidirectional coupling from the OB to dorsal and ventral HPC, indicating that, during odor processing, beta oscillations in the hippocampus are driven by the olfactory bulb.

Dopaminergic neuromodulation of synaptic transmission between mitral and granule cells in the teleost olfactory bulb

2012 ◽  
Vol 107 (5) ◽  
pp. 1313-1324 ◽  
Author(s):  
Takafumi Kawai ◽  
Hideki Abe ◽  
Yoshitaka Oka
Keyword(s):  
Olfactory Bulb ◽  
Synaptic Transmission ◽  
Granule Cells ◽  
Glutamate Release ◽  
Field Potential ◽  
Olfactory Nerve ◽  
Oscillatory Activity ◽  
Cellular Mechanisms ◽  
Olfactory Information

A growing body of evidence suggests that teleosts are important models for the study of neural processing of olfactory information, and the functional role of dopamine (DA), which is a potent neuromodulator endogenous to the mammalian olfactory bulb, has been one of the strongest focuses in this field. However, the cellular mechanisms of dopaminergic neuromodulation in olfactory bulbar neural circuits have not been fully understood. We investigated such mechanisms by using the goldfish, which offers several advantages for analyzing olfactory information processing by electrophysiological methods. First, we found in the olfactory bulb that numerous cell bodies of the dopaminergic neurons are mainly distributed in the mitral cell layer and extend fine processes to the glomerular layer. Next, we made in vitro field potential recordings and showed that synaptic transmissions from mitral to granule cells were suppressed by DA application. DA also increased the paired-pulse ratio, suggesting that the suppression of synaptic transmission is caused by a decrease in presynaptic glutamate release from the mitral cells. Furthermore, DA significantly suppressed the oscillatory activity of the olfactory bulb in response to olfactory stimuli. Although DA suppresses the synaptic inputs from the olfactory nerve to the olfactory bulbar neurons in mammals, this phenomenon was not observed in the goldfish. These findings indicate that suppression of the mitral to granule cell synaptic transmission in the reciprocal synapses plays an important role in the negative regulation of olfactory responsiveness in the goldfish olfactory bulb.

Increased Gamma Oscillatory Activity in the Subthalamic Nucleus During Tremor in Parkinson's Disease Patients

2009 ◽  
Vol 101 (2) ◽  
pp. 789-802 ◽  
Author(s):  
M. Weinberger ◽  
W. D. Hutchison ◽  
A. M. Lozano ◽  
M. Hodaie ◽  
J. O. Dostrovsky
Keyword(s):  
Parkinson’S Disease ◽  
Parkinson's Disease ◽  
Subthalamic Nucleus ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Neuronal Firing ◽  
Oscillatory Activity ◽  
Frequency Range ◽  
Resting Tremor ◽  
Gamma Frequency

Rest tremor is one of the main symptoms in Parkinson's disease (PD), although in contrast to rigidity and akinesia, the severity of the tremor does not correlate well with the degree of dopamine deficiency or the progression of the disease. Studies suggest that akinesia in PD patients is related to abnormal increased beta (15–30 Hz) and decreased gamma (35–80 Hz) synchronous oscillatory activity in the basal ganglia. Here we investigated the dynamics of oscillatory activity in the subthalamic nucleus (STN) during tremor. We used two adjacent microelectrodes to simultaneously record neuronal firing and local field potential (LFP) activity in nine PD patients who exhibited resting tremor during functional neurosurgery. We found that neurons exhibiting oscillatory activity at tremor frequency are located in the dorsal region of STN, where neurons with beta oscillatory activity are observed, and that their activity is coherent with LFP oscillations in the beta frequency range. Interestingly, in 85% of the 58 sites examined, the LFP exhibited increased oscillatory activity in the low gamma frequency range (35–55 Hz) during periods with stronger tremor. Furthermore, in 17 of 26 cases where two LFPs were recorded simultaneously, their coherence in the gamma range increased with increased tremor. When averaged across subjects, the ratio of the beta to gamma coherence was significantly lower in periods with stronger tremor compared with periods of no or weak tremor. These results suggest that resting tremor in PD is associated with an altered balance between beta and gamma oscillations in the motor circuits of STN.

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