Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice

Olfactory representations are shaped by both brain state and respiration; however, the interaction and circuit substrates of these influences are poorly understood. Granule cells (GCs) in the main olfactory bulb (MOB) are presumed to sculpt activity that reaches the olfactory cortex via inhibition of mitral/tufted cells (MTs). GCs may potentially sparsen ensemble activity by facilitating lateral inhibition among MTs, and/or they may enforce temporally-precise activity locked to breathing. Yet, the selectivity and temporal structure of GC activity during wakefulness are unknown. We recorded GCs in the MOB of anesthetized and awake mice and reveal pronounced state-dependent features of odor coding and temporal patterning. Under anesthesia, GCs exhibit sparse activity and are strongly and synchronously coupled to the respiratory cycle. Upon waking, GCs desynchronize, broaden their odor responses, and typically fire without regard for the respiratory rhythm. Thus during wakefulness, GCs exhibit stronger odor responses with less temporal structure. Based on these observations, we propose that during wakefulness GCs likely predominantly shape MT odor responses through broadened lateral interactions rather than respiratory synchronization.

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Brain-state dependent uncoupling of BOLD and local field potentials in laminar olfactory bulb

Neuroscience Letters ◽

10.1016/j.neulet.2014.07.034 ◽

2014 ◽

Vol 580 ◽

pp. 1-6 ◽

Cited By ~ 2

Author(s):

Ling Gong ◽

Bo Li ◽

Ruiqi Wu ◽

Anan Li ◽

Fuqiang Xu

Keyword(s):

Olfactory Bulb ◽

Local Field ◽

Local Field Potentials ◽

Brain State ◽

Field Potentials ◽

State Dependent

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State-dependent linearisation of mixture representations by the olfactory bulb

10.1101/2021.09.23.461425 ◽

2021 ◽

Author(s):

Aliya Mari Adefuin ◽

Janine K Reinert ◽

Sannder Lindeman ◽

Izumi Fukunaga

Keyword(s):

Olfactory Bulb ◽

Sensory Processing ◽

Piriform Cortex ◽

Brain State ◽

Complex Signals ◽

Two Photon ◽

State Dependent ◽

The Difference ◽

Apical Dendrites ◽

The Brain

Sensory systems are often tasked to analyse complex signals from the environment, to separate relevant from irrelevant parts. This process of decomposing signals is challenging when component signals interfere with each other. For example, when a mixture of signals does not equal the sum of its parts, this leads to an unpredictable corruption of signal patterns, making the target recognition harder. In olfaction, nonlinear summation is prevalent at various stages of sensory processing, from stimulus transduction in the nasal epithelium to higher areas, including the olfactory bulb (OB) and the piriform cortex. Here, we investigate how the olfactory system deals with binary mixtures of odours, using two-photon imaging with several behavioural paradigms. Unlike previous studies using anaesthetised animals, we found the mixture summation to be substantially more linear when using awake, head-fixed mice performing an odour detection task. This linearisation was also observed in awake, untrained mice, in both engaged and disengaged states, revealing that the bulk of the difference in mixture summation is explained by the brain state. However, in the apical dendrites of M/T cells, mixture representation is dominated by sublinear summation. Altogether, our results demonstrate that the property of mixture representation in the primary olfactory area likely reflects state-dependent differences in sensory processing.

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

Journal of Neurophysiology ◽

10.1152/jn.00623.2002 ◽

2003 ◽

Vol 90 (3) ◽

pp. 1921-1935 ◽

Cited By ~ 59

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.

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Top-down feedback enables flexible coding strategies in olfactory cortex

10.1101/2021.08.06.455459 ◽

2021 ◽

Author(s):

Zhen Chen ◽

Krishnan Padmanabhan

Keyword(s):

Olfactory Bulb ◽

Neural Activity ◽

Olfactory System ◽

Granule Cells ◽

Temporal Structure ◽

Time Windows ◽

Olfactory Cortex ◽

Top Down ◽

Cortical Cells ◽

Detailed Model

In chemical sensation, multiple models have been proposed to explain how odors are represented by patterns of neuronal activity in the olfactory cortex. One hypothesis is that the identity of combinations of active neurons within specific sniff-related time windows are critical for encoding information about odors. Another model is that patterns of neural activity evolve across time and it is this temporal structure that is essential for encoding odor information. Interestingly, we found that top-down feedback to the olfactory bulb dictates what information is transmitted to the olfactory cortex by switching between these two strategies. Using a detailed model of the early olfactory system, we demonstrate that feedback control of inhibitory granule cells in the main olfactory bulb influences the balance between excitatory and inhibitory synaptic currents in mitral cells, thereby restructuring the firing patterns of piriform cortical cells across time. This resulted in performance gains in both the accuracy and reaction time of odor discrimination tasks. These findings lead us to propose a new framework for early olfactory computation, one in which top-down feedback to the bulb flexibly controls the temporal structure of neural activity in olfactory cortex, allowing the early olfactory system to dynamically switch between two distinct models of coding.

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Propagation of Hippocampal Ripples to the Neocortex by Way of a Subiculum-Retrosplenial Pathway

10.1101/2020.02.27.966770 ◽

2020 ◽

Cited By ~ 1

Author(s):

Noam Nitzan ◽

Sam McKenzie ◽

Prateep Beed ◽

Daniel Fine English ◽

Silvia Oldani ◽

...

Keyword(s):

High Frequency ◽

Activity Patterns ◽

Retrosplenial Cortex ◽

Brain State ◽

Optogenetic Stimulation ◽

Sharp Wave ◽

State Dependent ◽

High Frequency Activity ◽

Underlying Mechanisms ◽

Ensemble Activity

SUMMARYBouts of high frequency activity known as sharp wave ripples (SPW-Rs) facilitate communication between the hippocampus and neocortex. However, the paths and mechanisms by which SPW-Rs broadcast their content are not well understood. Due to its anatomical positioning, the granular retrosplenial cortex (gRSC) may be a bridge for this hippocampo-cortical dialogue. Using silicon probe recordings in awake, head-fixed mice, we show the existence of SPW-R analogues in gRSC and demonstrate their coupling to hippocampal SPW-Rs. gRSC neurons reliably distinguished different subclasses of hippocampal SPW-Rs according to ensemble activity patterns in CA1. We demonstrate that this coupling is brain state-dependent, and delineate a topographically-organized anatomical pathway via VGlut2-expressing, bursty neurons in the subiculum. Optogenetic stimulation or inhibition of bursty subicular cells induced or reduced responses in superficial gRSC, respectively. These results identify a specific path and underlying mechanisms by which the hippocampus can convey neuronal content to the neocortex during SPW-Rs.

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Hippocampus: Intrinsic Organization

Handbook of Brain Microcircuits ◽

10.1093/med/9780190636111.003.0017 ◽

2017 ◽

pp. 199-216

Author(s):

Peter Somogyi ◽

Thomas Klausberger

Keyword(s):

Cerebral Cortex ◽

Granule Cells ◽

Pyramidal Cells ◽

Spike Timing ◽

Gabaergic Neurons ◽

Brain State ◽

Firing Rates ◽

State Dependent ◽

Postsynaptic Cell

The hippocampus, together with the subiculum, represent an associational area of the cerebral cortex that is intimately involved in mnemonic processes. Through its connections with other areas of the temporal lobe, the prefrontal cortex (PFC) and subcortical areas, it contributes to the encoding, association, consolidation, and recall of representations of the external and internal world in the combined firing rates and spike timing of glutamatergic pyramidal and granule cells. Pyramidal cell assemblies are formed and segregated from other assemblies by the dynamic strengthening and weakening of glutamatergic synaptic weights both on pyramidal cells and GABAergic interneurons. Interneurons, generate postsynaptic cell domain and brain state–dependent rhythmic changes in excitability, which are key for the formation, consolidation, and recall of representations. The chapter attempts to allocate explicit roles for some GABAergic neurons, based on their firing patterns in vivo as observed in identified neurons.

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Group I Metabotropic Glutamate Receptors Are Differentially Expressed by Two Populations of Olfactory Bulb Granule Cells

Journal of Neurophysiology ◽

10.1152/jn.01202.2006 ◽

2007 ◽

Vol 97 (4) ◽

pp. 3136-3141 ◽

Cited By ~ 8

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.

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Migration of bipolar subependymal cells, precursors of the granule cells of the rat olfactory bulb, with reference to the arrangement of the radial glial fibers.

Archives of Histology and Cytology ◽

10.1679/aohc.53.219 ◽

1990 ◽

Vol 53 (2) ◽

pp. 219-226 ◽

Cited By ~ 46

Author(s):

Kiyoshi KISHI ◽

Jun Yun PENG ◽

Sachiko KAKUTA ◽

Kunio MURAKAMI ◽

Masaru KURODA ◽

...

Keyword(s):

Olfactory Bulb ◽

Granule Cells ◽

Radial Glial

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The Mitral and Short Axon Cells of the Olfactory Bulb

Journal of Cell Science ◽

10.1242/jcs.7.3.631 ◽

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.

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