Ultrastructural analyses of local circuits in the olfactory system

1989 ◽  
Vol 47 ◽  
pp. 790-791
Author(s):  
C.A. Greer ◽  
C.K. Kaliszewski ◽  
H.A. Cameron
Keyword(s):  
Olfactory Bulb ◽  
High Voltage ◽  
Granule Cells ◽  
Sensory Information ◽  
Projection Neurons ◽  
Sprague Dawley ◽  
High Voltage Electron Microscopy ◽  
Tufted Cells ◽  
Local Circuits ◽  
Dendrodendritic Synapses

Information processing within the mammalian olfactory bulb, following transduction of odor stimuli by the receptor cells of the epithelium, occurs at two distinct levels. First, in the glomerular layer dendrodendritic synapses from a subpopulation of interneurons onto projection neurons (mitral and tufted cells) modulate the influence of arriving sensory information. The second level of processing occurs within the external plexiform layer where a second population of interneurons, granule cells, form reciprocal dendrodendritic synapses with mitral and tufted cells to modulate the flow of information out of the olfactory bulb. This second population of interneurons has been of interest, in part, due to the recent recognition that subpopulations form microcircuits preferentially with either the mitral or the tufted cell projection neurons, thus supporting the notion of parallel processing pathways. As part of a continuing effort to characterize the properties of these neurons and their dendritic circuits we have been utilizing light microscopy of selectively stained neurons and both conventional and high voltage electron microscopy of selectively stained neurons to study the geometry and synaptology of the olfactory bulb granule cells.Sprague-Dawley rats, 12 - 60 days postnatal, were perfused with 1% paraformaldehyde and 1% glutaraldehyde followed by immersion in the fixative for 8-12 hrs. After washes in 0.1M phosphate buffer the tissue was passed through a conventional dehydration series, embedded in EPON and routinely stained with uranyl acetate and lead citrate following sectioning. In addition, littermates were processed for Golgi-EM. Tissue examined utilizing conventional EM (60 - 100kV) was cut at approximately 70 nm and mounted on formvar slotted grids. Tissue examined utilizing high voltage EM (800 - 1000 kV) was cut at 1 - 5 um and mounted on mesh grids prior to carbon coating. Serial sections studied with conventional EM were reconstructed and morphometrically assessed utilizing a PC based 3D reconstruction program.

Presynaptic Muscarinic Receptors Enhance Glutamate Release at the Mitral/Tufted to Granule Cell Dendrodendritic Synapse in the Rat Main Olfactory Bulb

2009 ◽  
Vol 101 (4) ◽  
pp. 2052-2061 ◽  
Author(s):  
Ambarish S. Ghatpande ◽  
Alan Gelperin
Keyword(s):  
Olfactory Bulb ◽  
Granule Cell ◽  
Basal Forebrain ◽  
Granule Cells ◽  
Calcium Influx ◽  
Glutamate Release ◽  
Gaba Release ◽  
Cellular Mechanisms ◽  
Tufted Cells

The mammalian olfactory bulb receives multiple modulatory inputs, including a cholinergic input from the basal forebrain. Understanding the functional roles played by the cholinergic input requires an understanding of the cellular mechanisms it modulates. In an in vitro olfactory bulb slice preparation we demonstrate cholinergic muscarinic modulation of glutamate release onto granule cells that results in γ-aminobutyric acid (GABA) release onto mitral/tufted cells. We demonstrate that the broad-spectrum cholinergic agonist carbachol triggers glutamate release from mitral/tufted cells that activates both AMPA and NMDA receptors on granule cells. Activation of the granule cell glutamate receptors leads to calcium influx through voltage-gated calcium channels, resulting in spike-independent, asynchronous GABA release at reciprocal dendrodendritic synapses that granule cells form with mitral/tufted cells. This cholinergic modulation of glutamate release persists through much of postnatal bulbar development, suggesting a functional role for cholinergic inputs from the basal forebrain in bulbar processing of olfactory inputs and possibly in postnatal development of the olfactory bulb.

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.

Postnatal Neurogenesis in the Olfactory Bulb

2016 ◽  
Author(s):  
Aleksandra Polosukhina ◽  
Pierre-Marie Lledo
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Sensory Information ◽  
Adult Brain ◽  
Sensory Function ◽  
The Other ◽  
Forthcoming Article ◽  
Adult Born Neurons ◽  
Newborn Neurons ◽  
The Brain

This is an advance summary of a forthcoming article in the Oxford Research Encyclopedia of Neuroscience. Please check back later for the full article. In adult mammals, the olfactory bulb and the hippocampus are the regions in the brain that undergo continuous neurogenesis (production and recruitment of newborn neurons). While the other regions of the brain still retain a certain degree of plasticity after birth, they no longer can integrate new neurons. In rodents, thousands of adult-born neurons integrate into the bulb each day, and this process has been found to contribute not only to sensory function, but also to olfactory memory. This was a surprising finding, since historically the adult-brain has been viewed as a static organ. Understanding the process of regeneration of mature neurons in the brain has great potential for therapeutic applications. Consequently, this process of adult-neurogenesis has received widespread attention from clinicians and scientists. Neuroblasts bound for the olfactory bulb are produced in the subventricular zone of the lateral ventricle. Once they reach the olfactory bulb, they mostly develop into inhibitory interneurons called granule cells. Just after one month, about half of the adult-born neurons are eliminated, and the other half fully integrate and function in the olfactory bulb. These cells not only process information from the sensory neurons in the bulb, but also receive massive innervation from various regions of the brain, including the olfactory cortex, locus coeruleus, the horizontal limb of diagonal band of Broca, and the dorsal raphe nucleus. The sensory (bottom-up) and cortical (top-down) activity has been found to play a vital role in the adult-born granule cell survival. Though the exact purpose of these newborn neurons has not been identified, some emerging functions include maintenance of olfactory bulb circuitry, modulating sensory information, modulating olfactory learning, and memory.

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.

scholarly journals Spontaneous activity generated within the olfactory bulb establishes the discrete wiring of mitral cell dendrites

2019 ◽  
Author(s):  
Satoshi Fujimoto ◽  
Marcus N. Leiwe ◽  
Richi Sakaguchi ◽  
Yuko Muroyama ◽  
Reiko Kobayakawa ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Spontaneous Activity ◽  
Neuronal Activity ◽  
Primary Dendrite ◽  
Sensory Information ◽  
Mitral Cell ◽  
Network Activity ◽  
Mitral Cells ◽  
Tufted Cells

ABSTRACTIn the mouse olfactory bulb, sensory information detected by ∼1,000 types of olfactory sensory neurons (OSNs) is represented by the glomerular map. The second-order neurons, mitral and tufted cells, connect a single primary dendrite to one glomerulus. This forms discrete connectivity between the ∼1,000 types of input and output neurons. It has remained unknown how this discrete dendrite wiring is established during development. We found that genetically silencing neuronal activity in mitral cells, but not from OSNs, perturbs the dendrite pruning of mitral cells. In vivo calcium imaging of awake neonatal animals revealed two types of spontaneous neuronal activity in mitral/tufted cells, but not in OSNs. Pharmacological and knockout experiments revealed a role for glutamate and NMDARs. The genetic blockade of neurotransmission among mitral/tufted cells reduced spontaneous activity and perturbed dendrite wiring. Thus, spontaneous network activity generated within the olfactory bulb self-organizes the parallel discrete connections in the mouse olfactory system.

scholarly journals Distinct lateral inhibitory circuits drive parallel processing of sensory information in the mammalian olfactory bulb

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Matthew A Geramita ◽  
Shawn D Burton ◽  
Nathan N Urban
Keyword(s):  
Granule Cells ◽  
Sensory Information ◽  
Cell Types ◽  
Specific Stimulus ◽  
Inhibitory Circuits ◽  
Parallel Pathways ◽  
Common Strategy ◽  
Feature Selectivity ◽  
Tufted Cells ◽  
Stimulus Features

Splitting sensory information into parallel pathways is a common strategy in sensory systems. Yet, how circuits in these parallel pathways are composed to maintain or even enhance the encoding of specific stimulus features is poorly understood. Here, we have investigated the parallel pathways formed by mitral and tufted cells of the olfactory system in mice and characterized the emergence of feature selectivity in these cell types via distinct lateral inhibitory circuits. We find differences in activity-dependent lateral inhibition between mitral and tufted cells that likely reflect newly described differences in the activation of deep and superficial granule cells. Simulations show that these circuit-level differences allow mitral and tufted cells to best discriminate odors in separate concentration ranges, indicating that segregating information about different ranges of stimulus intensity may be an important function of these parallel sensory pathways.

scholarly journals Long-range GABAergic inhibition modulates spatiotemporal dynamics of the output neurons in the olfactory bulb

2020 ◽  
Author(s):  
Pablo S. Villar ◽  
Ruilong Hu ◽  
Ricardo C. Araneda
Keyword(s):  
Olfactory Bulb ◽  
Long Range ◽  
Granule Cells ◽  
Brain Slices ◽  
Gabaergic Neurons ◽  
Gabaergic Inhibition ◽  
Top Down ◽  
Local Interneurons ◽  
Output Neurons ◽  
Tufted Cells

SUMMARYLocal interneurons of the olfactory bulb (OB) are densely innervated by long-range GABAergic neurons from the basal forebrain (BF), suggesting that this top-down inhibition regulates early processing in the olfactory system. However, how GABAergic inputs modulate the OB output neurons, the mitral/tufted cells, is unknown. Here, in acute brain slices, we show that optogenetic activation of BF GABAergic inputs produced distinct local circuit effects that can influence the activity of mitral/tufted cells in the spatiotemporal domains. Activation of the GABAergic axons produced a fast disinhibition of mitral/tufted cells consistent with a rapid and synchronous release of GABA onto local interneurons in the glomerular and inframitral circuits of the OB, which also reduced the spike precision of mitral/tufted cells in response to simulated stimuli. In addition, BF GABAergic inhibition modulated local oscillations in a layer-specific manner. The intensity of locally evoked θ oscillations was decreased upon activation of top-down inhibition in the glomerular circuit, while evoked γ oscillations were reduced by inhibition of granule cells. Furthermore, BF GABAergic input reduced dendrodendritic inhibition in mitral/tufted cells. Together, these results suggest that long-range GABAergic neurons from the BF are well suited to influence temporal and spatial aspects of processing by OB circuits.

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