The Synaptology of the Granule Cells of the Olfactory Bulb

1970 ◽  
Vol 7 (1) ◽  
pp. 125-155
Author(s):  
J. L. PRICE ◽  
T. P. S POWELL
Keyword(s):  
Olfactory Bulb ◽  
Synaptic Vesicles ◽  
Granule Cells ◽  
Mitral Cell ◽  
Synaptic Membrane ◽  
Quantitative Evidence ◽  
Axon Terminals ◽  
Quantitative Measurements ◽  
Asymmetrical Synapse ◽  
Cell Somata

The synapses related to the granule cells of the olfactory bulb of rat brain have been studied in aldehyde-fixed material. The synapses can be divided into three classes: (1) those which have asymmetrical synaptic membrane thickenings and spheroidal synaptic vesicles; (2) those with symmetrical synaptic thickenings and flattened vesicles; and (3) the reciprocal synapses, one half of which (from mitral to granule cell) has an asymmetrical synaptic thickening associated with spheroidal vesicles, while the other half (from granule to mitral cell) has a symmetrical synaptic thickening and flattened vesicles. Qualitative observations, supported by preliminary quantitative measurements, suggest that it may be possible to divide both the spheroidal and flattened-vesicle types into two further varieties, on the basis of size, The smaller variety of spheroidal vesicles is found in most axon terminals, while the larger spheroidal vesicles are present in mitral cell dendrites and in some of the axon terminals. The flattened vesicles associated with symmetrical synapses which are oriented on to the granule cells are smaller than the spheroidal vesicles, but the flattened vesicles in the spines and gemmules of the granule cells are the same size or larger than the spheroidal vesicles. The division of flattened vesicles into two sizes is supported by statistical analysis of measurements of these vesicles, but because of difficulty in identifying the axon terminals with asymmetrical synapses there is no quantitative evidence for such a division of spheroidal vesicles. The asymmetrical synapses are found predominantly on spines, gemmules, and dendritic varicosities, although they are occasionally present on shafts of dendrites and on the cell somata. The symmetrical synapses are almost completely restricted to the shafts of the peripheral processes and the deep dendrites, and to the cell somata; only very rarely are synapses of this type found on spines, and then always in conjunction with an asymmetrical synapse.

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.

A Study of Terminal Degeneration in the Olfactory Bulb of the Rat

1972 ◽  
Vol 10 (3) ◽  
pp. 585-619
Author(s):  
A. J. PINCHING ◽  
T. P. S. POWELL
Keyword(s):  
Olfactory Bulb ◽  
Synaptic Cleft ◽  
Olfactory Nerve ◽  
Synaptic Membrane ◽  
Morphological Identification ◽  
Axon Terminals ◽  
Quantitative Characteristics ◽  
Terminal Degeneration ◽  
Qualitative And Quantitative Characteristics

An ultrastructural study of degeneration in axon terminals of the glomerular layer of the rat olfactory bulb is described, concentrating particularly on the sequence of degeneration in the olfactory nerve terminals and the long-term events in the degeneration process in several terminal types. Olfactory nerve terminal degeneration is divided into 5 stages, representing parts of the sequential changes taking place in the terminal after fibre section. The main features in the sequence are as follows: I. Swelling of the terminal and its vesicles. II. Initial shrinkage of the terminal, while vesicles remain swollen and some are distorted. III. Further shrinkage and darkening of the terminal, distortion of many of the vesicles and some mitochondrial swelling. IV. Extreme shrinkage of the terminal and loss of cytoplasmic detail; synaptic contact still intact or partially separated. V. Disappearance of the presynaptic terminal and persistence of the post-synaptic thickening. The validity of the observation of the persistence of post-synaptic membrane thickenings is considered and evidence adduced in its favour, both qualitative and quantitative. Characteristics of the newly apposed profiles are described, including cisternae and alveolate vesicles; the extracellular material of the synaptic cleft is considered in the light of its association with persisting thickenings. The relevance of these associated Structures is discussed in terms of function and development. Spontaneous degeneration of olfactory nerves and the degeneration of the vomeronasal nerves in the accessory olfactory bulb are described, as well as Stage V in the degeneration of other terminal types of the glomeruli, following various lesions; persistence of post-synaptic thickenings after the degeneration of terminals showing symmetrical membrane thickenings is included. Observations on the persistence of post-synaptic thickenings in various sites in the central and peripheral nervous systems are reviewed in the context of the present study; the problems arising out of the morphological identification of apposition or reinnervations are discussed.

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)

An Electron-Microscopic Study of the Termination of the Afferent Fibres to the Olfactory Bulb from the Cerebral Hemisphere

1970 ◽  
Vol 7 (1) ◽  
pp. 157-187
Author(s):  
J. L. PRICE ◽  
T. P. S. POWELL
Keyword(s):  
Olfactory Bulb ◽  
Cerebral Hemisphere ◽  
Granule Cells ◽  
Anterior Commissure ◽  
Plexiform Layer ◽  
Granule Cell Layer ◽  
Electron Microscopic ◽  
Anterior Olfactory Nucleus ◽  
Axon Terminals ◽  
Axon Collaterals

An experimental investigation has been made of the site and mode of termination of the 3 groups of afferent fibres to the olfactory bulb which come from more caudal parts of the cerebral hemisphere. Lesions have been placed in the relevant parts of the brain of the rat and the resulting degeneration of axon terminals in the olfactory bulb studied with the electron microscope. All 3 groups of these extrinsic afferent fibres end in asymmetrical synapses upon the granule cells, and they have a differential termination upon its various processes. The possibility that these fibres also end upon other cells in the bulb (particularly the short-axon and periglomerular cells) cannot be excluded. The centrifugal fibres end upon gemmules in the deep half of the external plexiform layer only; no degenerating terminals were found in relation to the glomeruli although degenerating centrifugal axons are present here. The fibres of the anterior commissure terminate upon spines and varicosities of the deep dendrites and upon somatic spines of the granule cells. After lesions of the anterior olfactory nucleus, degenerating terminals were found in the ipsilateral olfactory bulb, which could not be ascribed to the centrifugal fibres or to the fibres of the anterior commissure, as they ended upon the spines of peripheral processes in the granule cell layer, and upon gemmules in the superficial as well as in the deep half of the external plexiform layer. It is proposed that these terminals are those of the axon collaterals from the ipsilateral anterior olfactory nucleus. The axons which form symmetrical synapses, and many which form asymmetrical synapses, do not degenerate even after a lesion immediately behind the olfactory bulb, and are therefore intrinsic to the bulb. It is suggested that the axons which are associated with symmetrical synapses are those of the short-axon cells, and the asymmetrical synapses are formed by the axon collaterals of the mitral and tufted cells.

The Termination of Centrifugal Fibres in the Glomerular Layer of the Olfactory Bulb

1972 ◽  
Vol 10 (3) ◽  
pp. 621-635
Author(s):  
A. J. PINCHING ◽  
T. P. S. POWELL
Keyword(s):  
Electron Microscope ◽  
Olfactory Bulb ◽  
Mitral Cell ◽  
Lateral Olfactory Tract ◽  
Anterior Olfactory Nucleus ◽  
Axon Terminals ◽  
Glomerular Layer ◽  
Olfactory Tract ◽  
Functional Implications

The termination of the centrifugal fibres running in the lateral olfactory tract to the glomerular layer of the rat olfactory bulb has been determined with the electron microscope; this has been done with material perfused at various times after section of the lateral olfactory tract, as well as after a combination of this lesion with the long-term degeneration of olfactory nerves. The axon terminals are sparse at the glomerular level, but undergo typical degenerative changes; they are distributed solely in the periglomerular region and intermediate zone. The most common post-synaptic profiles are the processes of periglomerular cells, but a few centrifugal fibres terminate on short-axon, tufted and mitral cell dendrites. Evidence is produced to suggest that the anterior olfactory nucleus does not project as far as the glomerular layer. The findings are discussed in relation to previous studies with normal material and silver degeneration methods on similar experimental material; the functional implications of the centrifugal pathways in the bulb are briefly discussed.

scholarly journals Effect of intervening lesions on amino acid distributions in rat olfactory cortex and olfactory bulb.

1980 ◽  
Vol 28 (11) ◽  
pp. 1157-1169 ◽  
Author(s):  
D A Godfrey ◽  
C D Ross ◽  
J A Carter ◽  
O H Lowry ◽  
F M Matschinsky
Keyword(s):  
Amino Acids ◽  
Olfactory Bulb ◽  
Granule Cells ◽  
Anterior Commissure ◽  
Piriform Cortex ◽  
Mitral Cell ◽  
Olfactory Cortex ◽  
Gamma Aminobutyric Acid ◽  
Lateral Olfactory Tract ◽  
Mapping Procedure

Levels of the proposed neurotransmitter amino acids glutamate, aspartate, gamma-aminobutyric acid (GABA), and glycine were measured within the layered structures of the olfactory bulb and olfactory cortex following unilateral transections of the lateral olfactory tract or of virtually all fiber tracts of the olfactory peduncle. Distributions of the amino acids on both lesion and control sides were examined and compared by means of a mapping procedure. The results suggest: 1) Glutamate and aspartate are specifically associated with mitral (and presumably also tufted) cell axons and terminals in the piriform cortex. The distribution of aspartate in the olfactory bulb is further suggestive of a specific association of aspartate with mitral cell dendrites and somata. 2) Glutamate might be specifically associated with some centrifugal fibers traveling to the olfactory bulb in or near the anterior commissure. 3) GABA might be specifically related to some certrifugal fibers to the olfactory bulb in addition to its prominent association with granule cells of the bulb. 4) Glycine is unlikely to play a prominent neurotransmitter role in either the olfactory bulb or olfactory cortex.

Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation

1990 ◽  
Vol 64 (3) ◽  
pp. 932-947 ◽  
Author(s):  
D. P. Wellis ◽  
J. W. Scott
Keyword(s):  
Electrical Stimulation ◽  
Olfactory Bulb ◽  
Granule Cell ◽  
Action Potentials ◽  
Granule Cells ◽  
Olfactory Nerve ◽  
Mitral Cell ◽  
Intracellular Recordings ◽  
Postsynaptic Potential ◽  
Stimulation Of

1. Intracellular recordings were made from 28 granule cells and 6 periglomerular cells of the rat olfactory bulb during odor stimulation and electrical stimulation of the olfactory nerve layer (ONL) and lateral olfactory tract (LOT). Neurons were identified by injection of horseradish peroxidase (HRP) or biocytin and/or intracellular response characteristics. Odorants were presented in a cyclic sniff paradigm, as reported previously. 2. All interneurons could be activated from a wide number of stimulation sites on the ONL, with distances exceeding their known dendritic spreads and the dispersion of nerve fibers within the ONL, indicating that multisynaptic pathways must also exist at the glomerular region. All types of interneurons also responded to odorant stimulation, showing a variety of responses. 3. Granule cells responded to electrical stimulation of the LOT and ONL as reported previously. However, intracellular potential, excitability, and conductance analysis suggested that the mitral cell-mediated excitatory postsynaptic potential (EPSP) is followed by a long inhibitory postsynaptic potential (IPSP). An early negative potential, before the EPSP, was also observed in every granule cell and correlated with component I of the extracellular LOT-induced field potential. We have interpreted this negativity as a "field effect," that may be diagnostic of granule cells. 4. Most granule cells exhibited excitatory responses to odorant stimulation. Odors could produce spiking responses that were either nonhabituating (response to every sniff) or rapidly habituating (response to first sniff only). Other granule cells, while spiking to electrical stimulation, showed depolarizations that did not evoke spikes to odor stimulation. These depolarizations were transient with each sniff or sustained across a series of sniffs. These physiological differences to odor stimulation correlated with granule cell position beneath the mitral cell layer for 12 cells, suggesting that morphological subtypes of granule cells may show physiological differences. Some features of the granule cell odor responses seem to correlate with some of the features we have observed in mitral/tufted cell intracellular recordings. Only one cell showed inhibition to odors. 5. Periglomerular (PG) cells showed a response to ONL stimulation that was unlike that found in other olfactory bulb neurons. There was a long-duration hyperpolarization after a spike and large depolarization or burst of spikes (20-30 ms in duration). Odor stimulation produced simple bursts of action potentials, Odor stimulation produced simple bursts of action potentials, suggesting that PG cells may simply follow input from the olfactory nerve.(ABSTRACT TRUNCATED AT 400 WORDS)

SK Channel Regulation of Dendritic Excitability and Dendrodendritic Inhibition in the Olfactory Bulb

2005 ◽  
Vol 94 (6) ◽  
pp. 3743-3750 ◽  
Author(s):  
Brady J. Maher ◽  
Gary L. Westbrook
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Brain Slices ◽  
Mitral Cell ◽  
Mitral Cells ◽  
Sk Channels ◽  
Action Potential Firing ◽  
Sk Channel ◽  
Dendritic Excitability ◽  
Potential Firing

Small-conductance calcium-activated potassium channels (SK) regulate dendritic excitability in many neurons. In the olfactory bulb, regulation of backpropagating action potentials and dendrodendritic inhibition depend on the dendritic excitability of mitral cells. We report here that SK channel currents are present in mitral cells but are not detectable in granule cells in the olfactory bulb. In brain slices from PND 14–21 mice, long step depolarizations (100 ms) in the mitral cell soma evoked a cadmium- and apamin-sensitive outward SK current lasting several hundred milliseconds. Block of the SK current unmasked an inward N-methyl-d-aspartate (NMDA) autoreceptor current due to glutamate released from mitral cell dendrites. In low extracellular Mg2+ (100 μM), brief step depolarizations (2 ms) evoked an apamin-sensitive current that was reduced by d,l-2-amino-5-phosphonopentanoic acid. In current- clamp, block of SK channels increased action potential firing in mitral cells as well as dendrodendritic inhibition. Our results indicate that SK channels can be activated either by calcium channels or NMDA channels in mitral cell dendrites, providing a mechanism for local control of dendritic excitability.

Synaptic Organization and Neurotransmitters in the Rat Accessory Olfactory Bulb

1999 ◽  
Vol 81 (1) ◽  
pp. 345-355 ◽  
Author(s):  
Changping Jia ◽  
Wei R. Chen ◽  
Gordon M. Shepherd
Keyword(s):  
Olfactory Bulb ◽  
Granule Cells ◽  
Mitral Cell ◽  
Activity Period ◽  
Mitral Cells ◽  
Accessory Olfactory Bulb ◽  
Field Potentials ◽  
Synaptic Organization ◽  
Evoked Field Potentials ◽  
Stimulation Of

Jia, Changping, Wei R. Chen, and Gordon M. Shepherd. Synaptic organization and neurotransmitters in the rat accessory olfactory bulb. J. Neurophysiol. 81: 345–355, 1999. The accessory olfactory bulb (AOB) is the first relay station in the vomeronasal system and may play a critical role in processing pheromone signals. The AOB shows similar but less distinct lamination compared with the main olfactory bulb (MOB). In this study, synaptic organization of the AOB was analyzed in slice preparations from adult rats by using both field potential and patch-clamp recordings. Stimulation of the vomeronasal nerve (VN) evoked field potentials that showed characteristic patterns in different layers of the AOB. Current source density (CSD) analysis of the field potentials revealed spatiotemporally separated loci of inward current (sinks) that represented sequential activation of different neuronal components: VN activity (period I), synaptic excitation of mitral cell apical dendrites (period II), and activation of granule cells by mitral cell basal dendrites (period III). Stimulation of the lateral olfactory tract also evoked field potentials in the AOB, which indicated antidromic activation of the mitral cells (period I and II) followed by activation of granule cells (period III). Whole cell patch recordings from mitral and granule cells of the AOB supported that mitral cells are excited by VN terminals and subsequently activate granule cells through dendrodendritic synapses. Both CSD analysis and patch recordings provided evidence that glutamate is the neurotransmitter at the vomeronasal receptor neuron; mitral cell synapses and both NMDA and non-NMDA receptors are involved. We also demonstrated electrophysiologically that reciprocal interaction between mitral and granule cells in the AOB is through the dendrodendritic reciprocal synapses. The neurotransmitter at the mitral-to-granule synapses is glutamate and at the granule-to-mitral synapse is γ-aminobutyric acid. The synaptic interactions among receptor cell terminals, mitral cells, and granule cells in the AOB are therefore similar to those in the MOB, suggesting that processing of chemosensory information in the AOB shares similarities with that in the MOB.

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