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

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.

Download Full-text

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

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2020.614377 ◽

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.

Download Full-text

Olfactory Circuitry and Behavioral Decisions

Annual Review of Physiology ◽

10.1146/annurev-physiol-031820-092824 ◽

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.

Download Full-text

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

10.1101/135541 ◽

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.

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.2001.85.1.169 ◽

2001 ◽

Vol 85 (1) ◽

pp. 169-173 ◽

Cited By ~ 42

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.

Download Full-text

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

10.1101/625616 ◽

2019 ◽

Cited By ~ 7

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.

Download Full-text

Organization of inhibition in the rat olfactory bulb external plexiform layer

Journal of Neurophysiology ◽

10.1152/jn.1993.70.1.263 ◽

1993 ◽

Vol 70 (1) ◽

pp. 263-274 ◽

Cited By ~ 35

Author(s):

P. I. Ezeh ◽

D. P. Wellis ◽

J. W. Scott

Keyword(s):

Olfactory Bulb ◽

Plexiform Layer ◽

Type I ◽

Mitral Cells ◽

Type Ii ◽

Cell Responses ◽

Basal Dendrites ◽

Antidromic Stimulation ◽

Tufted Cells ◽

Stimulation Of

1. Intracellular recordings were made from the output neurons (mitral and tufted cells) of the rat olfactory bulb during electrical orthodromic stimulation of the olfactory nerve layer (ONL) and antidromic stimulation of the lateral olfactory tract and posterior piriform cortex (pPC) to test for physiological differences among the neuron types. Many of these neurons were identified by intracellular injections of biocytin, and others were identified by their pattern of antidromic activation. 2. Both marked and unmarked mitral cells showed large inhibitory postsynaptic potentials (IPSPs) in response to antidromic stimulation of the pPC, whereas tufted cells exhibited small IPSPs in response to pPC stimulation. Tufted cells, however, showed large IPSPs in response to ONL stimulation. In many cases, these tufted cell responses to ONL stimulation were larger than the mitral cell responses. The marked superficial tufted cells, those with basal dendrites in the superficial sublayer of the external plexiform layer (EPL), had the smallest IPSPs in response to pPC stimulation. These data support anatomic observations suggesting that the granule cell populations responsible for the IPSPs may be different for mitral and for superficial tufted cells. 3. The different types of output cells also showed differences in their responses to orthodromic stimulation. Type I mitral cells, which have basal dendrites confined to the deep sublayer of the EPL, were significantly less excitable by ONL stimulation than were the type II mitral cells, which have basal dendrites distributed within the intermediate sublayer of the EPL. Half of the type I mitral cells could not be excited at all by ONL stimulation. Superficial tufted cells showed even greater orthodromic excitability than type II mitral cells, usually responding to ONL stimulation with two or more spikes. 4. The ionic basis of the IPSPs in the superficial tufted cells appeared similar to those described for mitral cells. These IPSPs could be reversed by chloride injection and were associated with increased membrane conductance. 5. For both mitral and tufted cells, the number of ONL electrodes evoking IPSPs was greater than the number evoking spikes. These data suggest a kind of center-surround organization of inputs to these cells from the ONL, although this does not yet imply that the sensory receptive field of these output cells has a center-surround organization. 6. In conclusion, the properties of rat olfactory bulb output cells correlate with the sublayers of the EPL in which their basal dendrites lie.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Sniff rhythm-paced fast and slow gamma-oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states

Journal of Neurophysiology ◽

10.1152/jn.00379.2013 ◽

2013 ◽

Vol 110 (7) ◽

pp. 1593-1599 ◽

Cited By ~ 41

Author(s):

Hiroyuki Manabe ◽

Kensaku Mori

Keyword(s):

Olfactory Bulb ◽

Early Onset ◽

Transition Period ◽

Gamma Oscillations ◽

Projection Neurons ◽

Mitral Cells ◽

Behavioral States ◽

Tufted Cells ◽

Frequency Burst ◽

Odor Signals

Odor signals are conveyed from the olfactory bulb (OB) to the olfactory cortex by two types of projection neurons, tufted cells and mitral cells, which differ in signal timing and firing frequency in response to odor inhalation. Whereas tufted cells respond with early-onset high-frequency burst discharges starting at the middle of the inhalation phase of sniff, mitral cells show odor responses with later-onset lower-frequency burst discharges. Since odor inhalation induces prominent gamma-oscillations of local field potentials (LFPs) in the OB during the transition period from inhalation to exhalation that accompany synchronized spike discharges of tufted cells and mitral cells, we addressed the question of whether the odor-induced gamma-oscillations encompass two distinct gamma-oscillatory sources, tufted cell and mitral cell subsystems, by simultaneously recording the sniff rhythms and LFPs in the OB of freely behaving rats. We observed that individual sniffs induced nested gamma-oscillations with two distinct parts during the inhalation-exhalation transition period: early-onset fast gamma-oscillations followed by later-onset slow gamma-oscillations. These results suggest that tufted cells carry odor signals with early-onset fast gamma-synchronization at the early phase of sniff, whereas mitral cells send them with later-onset slow gamma-synchronization. We also observed that each sniff typically induced both fast and slow gamma-oscillations during awake, whereas respiration during slow-wave sleep and rapid-eye-movement sleep failed to induce these oscillations. These results suggest that behavioral states regulate the generation of sniff rhythm-paced fast and slow gamma-oscillations in the OB.

Download Full-text

The Neuron Types of the Glomerular Layer of the Olfactory Bulb

Journal of Cell Science ◽

10.1242/jcs.9.2.305 ◽

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.

Download Full-text

Mitral Cells of Olfactory Bulb Are Capable of Encoding Odor Location*

PROGRESS IN BIOCHEMISTRY AND BIOPHYSICS ◽

10.3724/sp.j.1206.2011.00173 ◽

2011 ◽

Vol 38 (11) ◽

pp. 1020-1026 ◽

Cited By ~ 1

Author(s):

Xiang LI ◽

An-An LI ◽

Ling GONG ◽

Qing LIU ◽

Fu-Qiang XU

Keyword(s):

Olfactory Bulb ◽

Mitral Cells

Download Full-text