Dendrodendritic Inhibition and Simulated Odor Responses in a Detailed Olfactory Bulb Network Model

2003 ◽  
Vol 90 (3) ◽  
pp. 1921-1935 ◽  
Author(s):  
Andrew P. Davison ◽  
Jianfeng Feng ◽  
David Brown
Keyword(s):  
Experimental Data ◽  
Spatial Distribution ◽  
Olfactory Bulb ◽  
Time Course ◽  
Granule Cells ◽  
Temporal Structure ◽  
Network Connectivity ◽  
Realistic Model ◽  
Mitral Cells ◽  
Dendrodendritic Synapses

In the olfactory bulb, both the spatial distribution and the temporal structure of neuronal activity appear to be important for processing odor information, but it is currently impossible to measure both of these simultaneously with high resolution and in all layers of the bulb. We have developed a biologically realistic model of the mammalian olfactory bulb, incorporating the mitral and granule cells and the dendrodendritic synapses between them, which allows us to observe the network behavior in detail. The cell models were based on previously published work. The attributes of the synapses were obtained from the literature. The pattern of synaptic connections was based on the limited experimental data in the literature on the statistics of connections between neurons in the bulb. The results of simulation experiments with electrical stimulation agree closely in most details with published experimental data. This gives confidence that the model is capturing features of network interactions in the real olfactory bulb. The model predicts that the time course of dendrodendritic inhibition is dependent on the network connectivity as well as on the intrinsic parameters of the synapses. In response to simulated odor stimulation, strongly activated mitral cells tend to suppress neighboring cells, the mitral cells readily synchronize their firing, and increasing the stimulus intensity increases the degree of synchronization. Preliminary experiments suggest that slow temporal changes in the degree of synchronization are more useful in distinguishing between very similar odorants than is the spatial distribution of mean firing rate.

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.

Exploring parameter space in detailed single neuron models: simulations of the mitral and granule cells of the olfactory bulb

1993 ◽  
Vol 69 (6) ◽  
pp. 1948-1965 ◽  
Author(s):  
U. S. Bhalla ◽  
J. M. Bower
Keyword(s):  
Experimental Data ◽  
Olfactory Bulb ◽  
Parameter Space ◽  
Potassium Current ◽  
Granule Cells ◽  
Cell Model ◽  
Mitral Cell ◽  
Delayed Rectifier ◽  
Model Output ◽  
Parameter Variations

1. Detailed compartmental computer simulations of single mitral and granule cells of the vertebrate olfactory bulb were constructed using previously published geometric data. Electrophysiological properties were determined by comparing model output to previously published experimental data, mainly current-clamp recordings. 2. The passive electrical properties of each model were explored by comparing model output with intracellular potential data from hyperpolarizing current injection experiments. The results suggest that membrane resistivity in both cells is nonuniform, with somatas having a substantially lower resistivity than the dendrites. 3. The active properties of these cells were explored by incorporating active ion channels into modeled compartments. On the basis of evidence from the literature, the mitral cell model included six channel types: fast sodium, fast delayed rectifier (Kfast), slow delayed rectifier (K), transient outward potassium current (KA), voltage- and calcium-dependent potassium current (KCa), and L-type calcium current. The granule cell model included four channel types: rat brain sodium, K, KA, and the non-inactivating muscarinic potassium current (KM). Modeled channels were based on the Hodgkin-Huxley formalism. 4. Representative kinetics for each of the channel classes above were obtained from the literature. The experimentally unknown spatial distributions of each included channel were obtained by systematic parameter searches. These were conducted in two ways: large-scale simulation series, in which each parameter was varied in turn, and an adaptation of a multidimensional conjugate gradient method. In each case, the simulated results were compared wtih experimental data using a curve-matching function evaluating mean squared differences of several aspects of the simulated and experimental voltage waveforms. 5. Systematic parameter variations revealed a single distinct region of parameter space in which the mitral cell model best fit the data. This region of parameter space was also very robust to parameter variations. Specifically, optimum performance was obtained when calcium and slow K channels were concentrated in the glomeruli, with a lower density in the soma and proximal secondary dendrites. The distribution of sodium and fast potassium channels, on the other hand, was highest at the soma and axon, with a much lighter distribution throughout the secondary dendrites. The KA and KCa channels were also concentrated near the soma. 6. The parameter search of the granule cell model was much less restrained by experimental data. Several parameter regimes were found that gave a good match to the data.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Spatial structure of synchronized inhibition in the olfactory bulb

2017 ◽  
Author(s):  
Hannah A. Arnson ◽  
Ben W. Strowbridge
Keyword(s):  
Olfactory Bulb ◽  
Action Potentials ◽  
Granule Cells ◽  
Gaba Release ◽  
Principal Cells ◽  
Receptor Neurons ◽  
Olfactory Bulb Slices ◽  
Cortical Regions ◽  
Large Groups ◽  
Dendrodendritic Synapses

AbstractOlfactory sensory input is detected by receptor neurons in the nose which then send information to the olfactory bulb, the first brain region for processing olfactory information. Within the olfactory bulb, many local circuit interneurons, including axonless granule cells, function to facilitate fine odor discrimination. How interneurons interact with principal cells to affect bulbar processing is not known though the mechanism is likely to be different than in sensory cortical regions since the olfactory bulb lacks an obvious topographical organization; neighboring glomerular columns, representing inputs from different receptor neuron subtypes, typically have different odor tuning. Determining the spatial scale over which interneurons such as granule cells can affect principal cells is a critical step towards understanding how the olfactory bulb operates. We addressed this question by assaying inhibitory synchrony using intracellular recordings from pairs of principal cells with different inter-somatic spacing. We find that in acute rat olfactory bulb slices, inhibitory synchrony is evident in the spontaneous synaptic input in mitral cells separated up to 300 μm. At all inter-somatic spacing assayed, inhibitory synchrony was dependent on fast Na+ channels, suggesting that action potentials in granule cells function to coordinate GABA release at relatively distant dendrodendritic synapses formed throughout the the dendritic arbor. Our results suggest that individual granule cells are able to influence relatively large groups of mitral and tufted cells belonging to clusters of at least 15 glomerular modules, providing a potential mechanism to integrate signals reflecting a wide variety of odorants.

scholarly journals Local postsynaptic signalling on slow time scales in reciprocal olfactory bulb granule cell spines matches asynchronous release

2020 ◽  
Author(s):  
Tiffany Ona Jodar ◽  
Vanessa Lage-Rupprecht ◽  
Nixon M. Abraham ◽  
Christine R. Rose ◽  
Veronica Egger
Keyword(s):  
Olfactory Bulb ◽  
Time Scales ◽  
Time Course ◽  
Granule Cells ◽  
Gaba Release ◽  
Fluorescence Signal ◽  
Slow Time ◽  
Triggered Release ◽  
Time To Peak ◽  
Adult Mice

AbstractIn the vertebrate olfactory bulb (OB), axonless granule cells (GC) mediate self- and lateral inhibitory interactions between mitral/tufted cells via reciprocal dendrodendritic synapses. Locally triggered release of GABA from the large reciprocal GC spines occurs on both fast and slow time scales, possibly enabling parallel processing during olfactory perception. Here we investigate local mechanisms for asynchronous spine output.To reveal the temporal and spatial characteristics of postsynaptic ion transients, we imaged spine and adjacent dendrite Ca2+- and Na+-signals with minimal exogenous buffering by the respective fluorescent indicator dyes upon two-photon uncaging of DNI-glutamate in OB slices from juvenile rats. Both postsynaptic fluorescence signals decayed slowly, with average half durations in the spine head of t1/2_Δ[Ca2+]i ~500 ms and t1/2_Δ[Na+]i ~1000 ms. We also analysed the kinetics of already existing data of postsynaptic spine Ca2+-signals in response to glomerular stimulation in OB slices from adult mice, either WT or animals with partial GC glutamate receptor deletions (NMDAR: GluN1 subunit; AMPAR: GluA2 subunit). In a large subset of spines the fluorescence signal had a protracted rise time (average time to peak ~400 ms, range 20 ms - >1000 ms). This slow rise was independent of Ca2+ entry via NMDARs, since similarly slow signals occurred in ΔGluN1 GCs. Additional Ca2+ entry in ΔGluA2 GCs (with AMPARs rendered Ca2+-permeable), however, resulted in larger ΔF/Fs that rose yet more slowly.Thus GC spines appear to dispose of several local mechanisms to promote asynchronous GABA release, which are reflected in the time course of mitral/tufted cell recurrent inhibition.

Tufted Cell Dendrodendritic Inhibition in the Olfactory Bulb Is Dependent on NMDA Receptor Activity

2001 ◽  
Vol 85 (1) ◽  
pp. 169-173 ◽  
Author(s):  
J. M. Christie ◽  
N. E. Schoppa ◽  
G. L. Westbrook
Keyword(s):  
Nmda Receptor ◽  
Olfactory Bulb ◽  
Plexiform Layer ◽  
Cell Voltage ◽  
Mitral Cells ◽  
Postsynaptic Currents ◽  
Tufted Cells ◽  
Primary Output ◽  
Sphere Of Influence ◽  
Dendrodendritic Synapses

Mitral and tufted cells constitute the primary output cells of the olfactory bulb. While tufted cells are often considered as “displaced” mitral cells, their actual role in olfactory bulb processing has been little explored. We examined dendrodendritic inhibition between tufted cells and interneurons using whole cell voltage-clamp recording. Dendrodendritic inhibitory postsynaptic currents (IPSCs) generated by depolarizing voltage steps in tufted cells were completely blocked by the N-methyl-d-aspartate (NMDA) receptor antagonistd,l-2amino-5-phosphonopentanoic acid (d,l-AP5), whereas the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor antagonist 2-3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f] quinoxaline-7-sulfonamide (NBQX) had no effect. Tufted cells in the external plexiform layer (EPL) and in the periglomerular region (PGR) showed similar behavior. These results indicate that NMDA receptor–mediated excitation of interneurons drives inhibition of tufted cells at dendrodendritic synapses as it does in mitral cells. However, the spatial extent of lateral inhibition in tufted cells was much more limited than in mitral cells. We suggest that the sphere of influence of tufted cells, while qualitatively similar to mitral cells, is centered on only one or a few glomeruli.

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