The Neuron Types of the Glomerular Layer of the Olfactory Bulb

1971 ◽  
Vol 9 (2) ◽  
pp. 305-345
Author(s):  
A. J. PINCHING ◽  
T. P. S. POWELL
Keyword(s):  
Olfactory Bulb ◽  
Structural Characteristics ◽  
Mitral Cells ◽  
Electron Microscopic ◽  
Nissl Staining ◽  
Axon Terminals ◽  
Glomerular Layer ◽  
Abundant Cytoplasm ◽  
Tufted Cells ◽  
Periglomerular Cells

The neurons of the glomerular layer of the rat olfactory bulb have been studied using Nissl staining and Golgi-Kopsch impregnation in light microscopy to define the size, shape and morphological features of individual cell somata, dendrites and axons; these have been correlated with electron-microscopic material in which fine-structural characteristics were also noted for each cell type, particularly synaptic specializations. Three neuron types are described: the external tufted and periglomerular cells of classical microscopy, and additional, superficial short-axon cells; a description of the glomerular arborizations of the mitral and deep tufted cells is also included. The tufted and mitral cells show large, non-spiny glomerular dendritic arborizations, having terminal varicosities, the external tufted cells being more limited in their branching than the deeper cells. External tufted cells have large somata and abundant cytoplasm containing stacks of Nissl material; their main dendrites are characterized by pale cytoplasm and a regular array of neurotubules. Reciprocal dendro-dendritic and somato-dendritic synapses are commonly found, the tufted/mitral cells containing spherical vesicles and contacting by means of asymmetrical membrane thickenings; the other profile involved is a gemmule containing large flattened vesicles and associated with a symmetrical thickening. The periglomerular cells are smaller, with a spiny glomerular arborization, as well as some other dendrites; all the dendrites of these cells tend to be of irregular outline. They have a dark nucleus and very little somatic cytoplasm; somatic and dendritic appendages are common and often contain large flattened vesicles. Synapses oriented from the dendritic shaft or gemmule also show such vesicles, invariably associated with symmetrical thickenings. The superficial short-axon cells are characterized by the entirely periglomerular distribution of their dendrites, which are varicose and rarely branch. Of intermediate soma dimensions, but containing dispersed Nissl material, these cells and their stem dendrites show no regions that can be designated as presynaptic. Features of axon initial segments, axo-somatic and axo-dendritic synapses are also described for each cell, as well as some unusual glial relationships. Reasons are adduced for relating the superficial short-axon cell to the axon terminal type containing small flattened vesicles, as well as for considering that the external tufted and periglomerular cells show the same synaptic specializations at their axon terminals as at their dendritic and somatic synapses. The cells of the glomerular layer are compared with those of the deeper layers of the bulb and atypical synaptic specializations discussed; some physiological implications of these findings are considered.

Mitral and Tufted Cells Differ in the Decoding Manner of Odor Maps in the Rat Olfactory Bulb

2004 ◽  
Vol 91 (6) ◽  
pp. 2532-2540 ◽  
Author(s):  
Shin Nagayama ◽  
Yuji K. Takahashi ◽  
Yoshihiro Yoshihara ◽  
Kensaku Mori
Keyword(s):  
Olfactory Bulb ◽  
Spike Activity ◽  
Homologous Series ◽  
Morphological Difference ◽  
Aliphatic Acid ◽  
Mitral Cells ◽  
Firing Rates ◽  
Aliphatic Acids ◽  
Projection Pattern ◽  
Tufted Cells

Mitral and tufted cells in the mammalian olfactory bulb are principal neurons, each type having distinct projection pattern of their dendrites and axons. The morphological difference suggests that mitral and tufted cells are functionally distinct and may process different aspects of olfactory information. To examine this possibility, we recorded odorant-evoked spike responses from mitral and middle tufted cells in the aliphatic acid- and aldehyde-responsive cluster at the dorsomedial part of the rat olfactory bulb. Homologous series of aliphatic acids and aldehydes were used for odorant stimulation. In response to adequate odorants, mitral cells showed spike responses with relatively low firing rates, whereas middle tufted cells responded with higher firing rates. Examination of the molecular receptive range (MRR) indicated that most mitral cells exhibited a robust inhibitory MRR, whereas a majority of middle tufted cells showed no or only a weak inhibitory MRR. In addition, structurally different odorants that activated neighboring clusters inhibited the spike activity of mitral cells, whereas they caused no or only a weak inhibition in the middle tufted cells. Furthermore, responses of mitral cells to an adequate excitatory odorant were greatly inhibited by mixing the odorant with other odorants that activated neighboring glomeruli. In contrast, odorants that activated neighboring glomeruli did not significantly inhibit the responses of middle tufted cells to the adequate excitatory odorant. These results indicate a clear difference between mitral and middle tufted cells in the manner of decoding the glomerular odor maps.

scholarly journals Cellular and Synaptic Mechanisms That Differentiate Mitral Cells and Superficial Tufted Cells Into Parallel Output Channels in the Olfactory Bulb

2020 ◽  
Vol 14 ◽  
Author(s):  
Shelly Jones ◽  
Joel Zylberberg ◽  
Nathan Schoppa
Keyword(s):  
Olfactory Bulb ◽  
Plexiform Layer ◽  
Input Resistance ◽  
Cell Types ◽  
Mitral Cells ◽  
Whole Cell ◽  
Wide Range ◽  
Tufted Cells ◽  
Parallel Output

A common feature of the primary processing structures of sensory systems is the presence of parallel output “channels” that convey different information about a stimulus. In the mammalian olfactory bulb, this is reflected in the mitral cells (MCs) and tufted cells (TCs) that have differing sensitivities to odors, with TCs being more sensitive than MCs. In this study, we examined potential mechanisms underlying the different responses of MCs vs. TCs. For TCs, we focused on superficial TCs (sTCs), which are a population of output TCs that reside in the superficial-most portion of the external plexiform layer, along with external tufted cells (eTCs), which are glutamatergic interneurons in the glomerular layer. Using whole-cell patch-clamp recordings in mouse bulb slices, we first measured excitatory currents in MCs, sTCs, and eTCs following olfactory sensory neuron (OSN) stimulation, separating the responses into a fast, monosynaptic component reflecting direct inputs from OSNs and a prolonged component partially reflecting eTC-mediated feedforward excitation. Responses were measured to a wide range of OSN stimulation intensities, simulating the different levels of OSN activity that would be expected to be produced by varying odor concentrations in vivo. Over a range of stimulation intensities, we found that the monosynaptic current varied significantly between the cell types, in the order of eTC > sTC > MC. The prolonged component was smaller in sTCs vs. both MCs and eTCs. sTCs also had much higher whole-cell input resistances than MCs, reflecting their smaller size and greater membrane resistivity. To evaluate how these different electrophysiological aspects contributed to spiking of the output MCs and sTCs, we used computational modeling. By exchanging the different cell properties in our modeled MCs and sTCs, we could evaluate each property's contribution to spiking differences between these cell types. This analysis suggested that the higher sensitivity of spiking in sTCs vs. MCs reflected both their larger monosynaptic OSN signal as well as their higher input resistance, while their smaller prolonged currents had a modest opposing effect. Taken together, our results indicate that both synaptic and intrinsic cellular features contribute to the production of parallel output channels in the olfactory bulb.

Olfactory Circuitry and Behavioral Decisions

2020 ◽  
Vol 83 (1) ◽  
Author(s):  
Kensaku Mori ◽  
Hitoshi Sakano
Keyword(s):  
Olfactory Bulb ◽  
Behavioral Responses ◽  
Olfactory Cortex ◽  
Annual Review ◽  
Publication Date ◽  
Mitral Cells ◽  
Topographic Map ◽  
Input Signals ◽  
Tufted Cells ◽  
Odor Signals

In mammals, odor information detected by olfactory sensory neurons is converted to a topographic map of activated glomeruli in the olfactory bulb. Mitral cells and tufted cells transmit signals sequentially to the olfactory cortex for behavioral outputs. To elicit innate behavioral responses, odor signals are directly transmitted by distinct subsets of mitral cells from particular functional domains in the olfactory bulb to specific amygdala nuclei. As for the learned decisions, input signals are conveyed by tufted cells as well as by mitral cells to the olfactory cortex. Behavioral scene cells link the odor information to the valence cells in the amygdala to elicit memory-based behavioral responses. Olfactory decision and perception take place in relation to the respiratory cycle. How is the sensory quality imposed on the olfactory inputs for behavioral outputs? How are the two types of odor signals, innate and learned, processed during respiration? Here, we review recent progress on the study of neural circuits involved in decision making in the mouse olfactory system. Expected final online publication date for the Annual Review of Physiology, Volume 83 is February 10, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Distinct temporal filters in mitral cells and external tufted cells of the olfactory bulb

2017 ◽  
Vol 595 (19) ◽  
pp. 6349-6362 ◽  
Author(s):  
Christopher E. Vaaga ◽  
Gary L. Westbrook
Keyword(s):  
Olfactory Bulb ◽  
Mitral Cells ◽  
Tufted Cells

scholarly journals Distinct Temporal Filters In Mitral Cells And External Tufted Cells Of The Olfactory Bulb

2017 ◽  
Author(s):  
Christopher E. Vaaga ◽  
Gary L. Westbrook
Keyword(s):  
Olfactory Bulb ◽  
High Frequency ◽  
Synaptic Depression ◽  
High Frequency Stimulation ◽  
Mitral Cells ◽  
Release Probability ◽  
High Release ◽  
Frequency Stimulation ◽  
Tufted Cells ◽  
Synaptic Dynamics

Short-term synaptic plasticity is a critical regulator of neural circuits, and largely determines how information is temporally processed. In the olfactory bulb, afferent olfactory receptor neurons respond to increasing concentrations of odorants with barrages of action potentials, and their terminals have an extraordinarily high release probability (Sicard, 1986; Murphy et al., 2004). These features suggest that during naturalistic stimuli, afferent input to the olfactory bulb is subject to strong synaptic depression, presumably truncating the postsynaptic response to afferent stimuli. To examine this issue, we used single glomerular stimulation in mouse olfactory bulb slices to measure the synaptic dynamics of afferent-evoked input at physiological stimulus frequencies. In cell-attached recordings, mitral cells responded to high frequency stimulation with sustained responses, whereas external tufted cells responded transiently. Consistent with previous reports (Murphy et al., 2004), olfactory nerve terminals onto both cell types had a high release probability (0.7), from a single pool of slowly recycling vesicles, indicating that the distinct responses of mitral and external tufted cells to high frequency stimulation did not originate presyaptically. Rather, distinct temporal response profiles in mitral cells and external tufted cells could be attributed to slow dendrodendritic responses in mitral cells, as blocking this slow current in mitral cells converted mitral cell responses to a transient response profile, typical of external tufted cells. Our results suggest that despite strong axodendritic synaptic depression, the balance of axodendritic and dendrodendritic circuitry in external tufted cells and mitral cells, respectively, tunes the postsynaptic responses to high frequency, naturalistic stimulation.

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.

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.

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.

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.

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