scholarly journals Connectivity and dynamics in the olfactory bulb

2021 ◽  
Author(s):  
David EC Kersen ◽  
Gaia Tavoni ◽  
Vijay Balasubramanian
Keyword(s):  
Olfactory Bulb ◽  
Lateral Inhibition ◽  
Large Scale ◽  
Computational Models ◽  
Granule Cells ◽  
Cell Activity ◽  
Gamma Oscillations ◽  
Scale Model ◽  
Mitral Cells ◽  
Cortical Feedback

Dendrodendritic interactions between excitatory mitral cells and inhibitory granule cells in the olfactory bulb create a dense interaction network, reorganizing sensory representations of odors and, consequently, perception. Large-scale computational models are needed for revealing how the collective behavior of this network emerges from its global architecture. We propose an approach where we summarize anatomical information through dendritic geometry and density distributions which we use to calculate the probability of synapse between mitral and granule cells, while capturing activity patterns of each cell type in the neural dynamical systems theory of Izhikevich. In this way, we generate an efficient, anatomically and physiologically realistic large-scale model of the olfactory bulb network. Our model reproduces known connectivity between sister vs. non-sister mitral cells; measured patterns of lateral inhibition; and theta, beta, and gamma oscillations. It in turn predicts testable relations between network structure, lateral inhibition, and odor pattern decorrelation; between the density of granule cell activity and LFP oscillation frequency; how cortical feedback to granule cells affects mitral cell activity; and how cortical feedback to mitral cells is modulated by the network embedding. Additionally, the methodology we describe here provides a tractable tool for other researchers.

Dynamical Mechanisms of Odor Processing in Olfactory Bulb Mitral Cells

2006 ◽  
Vol 96 (2) ◽  
pp. 555-568 ◽  
Author(s):  
Daniel B. Rubin ◽  
Thomas A. Cleland
Keyword(s):  
Olfactory Bulb ◽  
Large Scale ◽  
Computational Models ◽  
Potassium Conductance ◽  
Membrane Dynamics ◽  
Inhibitory Input ◽  
Mitral Cells ◽  
Hypoxic Conditions ◽  
Subthreshold Oscillations ◽  
Dynamical Properties

In the olfactory system, the contribution of dynamical properties such as neuronal oscillations and spike synchronization to the representation of odor stimuli is a matter of substantial debate. While relatively simple computational models have sufficed to guide current research in large-scale network dynamics, less attention has been paid to modeling the membrane dynamics in bulbar neurons that may be equally essential to sensory processing. We here present a reduced, conductance-based compartmental model of olfactory bulb mitral cells that exhibits the complex dynamical properties observed in these neurons. Specifically, model neurons exhibit intrinsic subthreshold oscillations with voltage-dependent frequencies that shape the timing of stimulus-evoked action potentials. These oscillations rely on a persistent sodium conductance, an inactivating potassium conductance, and a calcium-dependent potassium conductance and are reset via inhibitory input such as that delivered by periglomerular cell shunt inhibition. Mitral cells fire bursts, or clusters, of spikes when continuously stimulated. Burst properties depend critically on multiple currents, but a progressive deinactivation of IA over the course of a burst is an important regulator of burst termination. Each of these complex properties exhibits appropriate dynamics and pharmacology as determined by electrophysiological studies. Additionally, we propose that a second, inconsistently observed form of infrathreshold bistability in mitral cells may derive from the activation of ATP-activated potassium currents responding to hypoxic conditions. We discuss the integration of these cellular properties in the larger context of olfactory bulb network operations.

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.

γ-Frequency Excitatory Input to Granule Cells Facilitates Dendrodendritic Inhibition in the Rat Olfactory Bulb

2003 ◽  
Vol 90 (2) ◽  
pp. 644-654 ◽  
Author(s):  
Brian Halabisky ◽  
Ben W. Strowbridge
Keyword(s):  
Olfactory Bulb ◽  
Nmda Receptors ◽  
Lateral Inhibition ◽  
Granule Cells ◽  
Critical Role ◽  
Recurrent Inhibition ◽  
Granule Cell Layer ◽  
Gabaergic Interneurons ◽  
Mitral Cells ◽  
Dendrodendritic Synapses

Recurrent and lateral inhibition play a prominent role in patterning the odor-evoked discharges in mitral cells, the output neurons of the olfactory bulb. Inhibitory responses in this brain region are mediated through reciprocal synaptic connections made between the dendrites of mitral cells and GABAergic interneurons. Previous studies have demonstrated that N-methyl-d-aspartate (NMDA) receptors on interneurons play a critical role in eliciting GABA release at reciprocal dendrodendritic synapses. In acute olfactory bulb slices, these receptors are tonically blocked by extracellular Mg2+, and recurrent inhibition is disabled. In the present study, we examined the mechanisms by which this tonic blockade could be reversed. We demonstrate that near-coincident activation of an excitatory pathway to the proximal dendrites of GABAergic interneurons relieves the Mg2+ blockade of NMDA receptors at reciprocal dendrodendritic synapses and greatly facilitates recurrent inhibition onto mitral cells. Gating of recurrent and lateral inhibition in the presence of extracellular Mg2+ requires γ-frequency stimulation of glutamatergic axons in the granule cell layer. Long-range excitatory axon connections from mitral cells innervated by different subpopulations of olfactory receptor neurons may provide a gating input to granule cells, thereby facilitating the mitral cell lateral inhibition that contributes to odorant encoding.

Group I Metabotropic Glutamate Receptors Are Differentially Expressed by Two Populations of Olfactory Bulb Granule Cells

2007 ◽  
Vol 97 (4) ◽  
pp. 3136-3141 ◽  
Author(s):  
Thomas Heinbockel ◽  
Kathryn A. Hamilton ◽  
Matthew Ennis
Keyword(s):  
Olfactory Bulb ◽  
Glutamate Receptors ◽  
Metabotropic Glutamate Receptors ◽  
Granule Cells ◽  
Mitral Cell ◽  
Mitral Cells ◽  
Patch Clamp Recording ◽  
Metabotropic Glutamate ◽  
Group I ◽  
Bath Application

In the main olfactory bulb, several populations of granule cells (GCs) can be distinguished based on the soma location either superficially, interspersed with mitral cells within the mitral cell layer (MCL), or deeper, within the GC layer (GCL). Little is known about the physiological properties of superficial GCs (sGCs) versus deep GCs (dGCs). Here, we used patch-clamp recording methods to explore the role of Group I metabotropic glutamate receptors (mGluRs) in regulating the activity of GCs in slices from wildtype and mGluR−/− mutant mice. In wildtype mice, bath application of the selective Group I mGluR agonist DHPG depolarized and increased the firing rate of both GC subtypes. In the presence of blockers of fast synaptic transmission (APV, CNQX, gabazine), DHPG directly depolarized both GC subtypes, although the two GC subtypes responded differentially to DHPG in mGluR1−/− and mGluR5−/− mice. DHPG depolarized sGCs in slices from mGluR5−/− mice, although it had no effect on sGCs in slices from mGluR1−/− mice. By contrast, DHPG depolarized dGCs in slices from mGluR1−/− mice but had no effect on dGCs in slices from mGluR5−/− mice. Previous studies showed that mitral cells express mGluR1 but not mGluR5. The present results therefore suggest that sGCs are more similar to mitral cells than dGCs in terms of mGluR expression.

The Mitral and Short Axon Cells of the Olfactory Bulb

1970 ◽  
Vol 7 (3) ◽  
pp. 631-651
Author(s):  
J. L. PRICE ◽  
T. P. S. POWELL
Keyword(s):  
Electron Microscope ◽  
Olfactory Bulb ◽  
Granule Cells ◽  
Primary Dendrite ◽  
Plexiform Layer ◽  
Mitral Cell ◽  
Granule Cell Layer ◽  
Mitral Cells ◽  
Axon Initial Segments ◽  
Large Neurons

A description is given of the mitral and short axon cells of the olfactory bulb of the rat from Golgi material examined with the light microscope and from material examined with the electron microscope. The mitral cells are large neurons with primary and secondary dendrites which both extend into the overlying external plexiform layer, although only the primary dendrite enters the glomerular formations. No predominant antero-posterior orientation of the secondary dendrites has been found. Within the glomeruli the mitral cell dendrites are in synaptic contact with the olfactory nerves and also with the periglomerular cells, but elsewhere the only synapses on the mitral cells are the ‘reciprocal synapses’ with the granule cells. Synaptic-type vesicles are found in all parts of the mitral cells, including the axon initial segments; they appear to be especially concentrated in the distal portions of the dendrites. Several types of short axon cells have been found in the granule cell layer in Golgi-impregnated material. Their cell bodies can also be distinguished with the electron microscope, and from previous work it is probable that the axons of at least some of these cells form flattened-vesicle symmetrical synapses upon the granule cells.

Circuit Properties Generating Gamma Oscillations in a Network Model of the Olfactory Bulb

2006 ◽  
Vol 95 (4) ◽  
pp. 2678-2691 ◽  
Author(s):  
Brice Bathellier ◽  
Samuel Lagier ◽  
Philippe Faure ◽  
Pierre-Marie Lledo
Keyword(s):  
Olfactory Bulb ◽  
Firing Rate ◽  
Lateral Inhibition ◽  
Temporal Structure ◽  
Gamma Oscillations ◽  
Synaptic Organization ◽  
Neural Basis ◽  
Sensory Inputs ◽  
Model Based

The study of the neural basis of olfaction is important both for understanding the sense of smell and for understanding the mechanisms of neural computation. In the olfactory bulb (OB), the spatial patterning of both sensory inputs and synaptic interactions is crucial for processing odor information, although this patterning alone is not sufficient. Recent studies have suggested that representations of odor may already be distributed and dynamic in the first olfactory relay. The growing evidence demonstrating a functional role for the temporal structure of bulbar neuronal activity supports this assumption. However, the detailed mechanisms underlying this temporal structure have never been thoroughly studied. Our study focused on gamma (40–100 Hz) network oscillations in the mammalian OB, which is a form of temporal patterning in bulbar activity elicited by olfactory stimuli. We used computational modeling combined with electrophysiological recordings to investigate the basic synaptic organization necessary and sufficient to generate sustained gamma rhythms. We found that features of gamma oscillations obtained in vitro were identical to those of a model based on lateral inhibition as the coupling modality (i.e., low irregular firing rate and high oscillation stability). In contrast, they differed substantially from those of a model based on lateral excitatory coupling (i.e., high regular firing rate and instable oscillations). Therefore we could precisely tune the oscillation frequency by changing the kinetics of inhibitory events supporting the lateral inhibition. Moreover, gradually decreasing GABAergic synaptic transmission decreased the degree of relay neuron synchronization in response to sensory inputs, both theoretically and experimentally. Thus we have shown that lateral inhibition provides a mechanism by which the dynamic processing of odor information might be finely tuned within the OB circuit.

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 Short-Term Plasticity in Cortical GABAergic Synapses on Olfactory Bulb Granule Cells Is Modulated by Endocannabinoids

2021 ◽  
Vol 15 ◽  
Author(s):  
Fu-Wen Zhou ◽  
Adam C. Puche
Keyword(s):  
Olfactory Bulb ◽  
Sensory Processing ◽  
Granule Cell ◽  
Granule Cells ◽  
Cb1 Receptor ◽  
Granule Cell Layer ◽  
Short Term ◽  
Frequency Dependent ◽  
Short Term Plasticity ◽  
Cortical Feedback

Olfactory bulb and higher processing areas are synaptically interconnected, providing rapid regulation of olfactory bulb circuit dynamics and sensory processing. Short-term plasticity changes at any of these synapses could modulate sensory processing and potentially short-term sensory memory. A key olfactory bulb circuit for mediating cortical feedback modulation is granule cells, which are targeted by multiple cortical regions including both glutamatergic excitatory inputs and GABAergic inhibitory inputs. There is robust endocannabinoid modulation of excitatory inputs to granule cells and here we explored whether there was also endocannabinoid modulation of the inhibitory cortical inputs to granule cells. We expressed light-gated cation channel channelrhodopsin-2 (ChR2) in GABAergic neurons in the horizontal limb of the diagonal band of Broca (HDB) and their projections to granule cells in olfactory bulb. Selective optical activation of ChR2 positive axons/terminals generated strong, frequency-dependent short-term depression of GABAA-mediated-IPSC in granule cells. As cannabinoid type 1 (CB1) receptor is heavily expressed in olfactory bulb granule cell layer (GCL) and there is endogenous endocannabinoid release in GCL, we investigated whether activation of CB1 receptor modulated the HDB IPSC and short-term depression at the HDB→granule cell synapse. Activation of the CB1 receptor by the exogenous agonist Win 55,212-2 significantly decreased the peak amplitude of individual IPSC and decreased short-term depression, while blockade of the CB1 receptor by AM 251 slightly increased individual IPSCs and increased short-term depression. Thus, we conclude that there is tonic endocannabinoid activation of the GABAergic projections of the HDB to granule cells, similar to the modulation observed with glutamatergic projections to granule cells. Modulation of inhibitory synaptic currents and frequency-dependent short-term depression could regulate the precise balance of cortical feedback excitation and inhibition of granule cells leading to changes in granule cell mediated inhibition of olfactory bulb output to higher processing areas.

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