Temporal Dynamics of Inhalation-Linked Activity across Defined Subpopulations of Mouse Olfactory Bulb Neurons Imaged<i>In Vivo</i>

Short, Shaina M.; Wachowiak, Matt

doi:10.1523/eneuro.0189-19.2019

Cited by 27 publications

(35 citation statements)

References 61 publications

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“…To date, sniff-coupled activity in MCs and TCs has been described using both electrophysiological (Adrian, 1950 ; Cang and Isaacson, 2003 ; Margrie and Schaefer, 2003 ; Carey and Wachowiak, 2011 ; Shusterman et al, 2011 ; Smear et al, 2011 ; Fukunaga et al, 2012 , 2014 ; Igarashi et al, 2012 ; Díaz-quesada et al, 2018 ; Jordan et al, 2018a , b ) and imaging techniques (Iwata et al, 2017 ; Short and Wachowiak, 2019 ; Eiting and Wachowiak, 2020 ) in a variety of brain states. However, it is unclear how sniff-locking under wide-ranging protocols relates to each other, especially given that parameters of sniff patterns, or inputs to the olfactory system, can change drastically between anesthetized and awake states (Welker, 1964 ; Jessberger et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Respiration-Locking of Olfactory Receptor and Projection Neurons in the Mouse Olfactory Bulb and Its Modulation by Brain State

Ackels

Jordan

Schaefer

et al. 2020

Front. Cell. Neurosci.

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For sensory systems of the brain, the dynamics of an animal's own sampling behavior has a direct consequence on ensuing computations. This is particularly the case for mammalian olfaction, where a rhythmic flow of air over the nasal epithelium entrains activity in olfactory system neurons in a phenomenon known as sniff-locking. Parameters of sniffing can, however, change drastically with brain states. Coupled to the fact that different observation methods have different kinetics, consensus on the sniff-locking properties of neurons is lacking. To address this, we investigated the sniff-related activity of olfactory sensory neurons (OSNs), as well as the principal neurons of the olfactory bulb (OB), using 2-photon calcium imaging and intracellular whole-cell patch-clamp recordings in vivo, both in anesthetized and awake mice. Our results indicate that OSNs and OB output neurons lock robustly to the sniff rhythm, but with a slight temporal shift between behavioral states. We also observed a slight delay between methods. Further, the divergent sniff-locking by tufted cells (TCs) and mitral cells (MCs) in the absence of odor can be used to determine the cell type reliably using a simple linear classifier. Using this classification on datasets where morphological identification is unavailable, we find that MCs use a wider range of temporal shifts to encode odors than previously thought, while TCs have a constrained timing of activation due to an early-onset hyperpolarization. We conclude that the sniff rhythm serves as a fundamental rhythm but its impact on odor encoding depends on cell type, and this difference is accentuated in awake mice.

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Section: Introductionmentioning

confidence: 99%

Respiration-Locking of Olfactory Receptor and Projection Neurons in the Mouse Olfactory Bulb and Its Modulation by Brain State

Ackels

Jordan

Schaefer

et al. 2020

Front. Cell. Neurosci.

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“…This renewed interest in the coordination of rodent orofacial motor behaviors has led to the development of novel technologies for measuring rodent breathing and sniffing [19,20], which are complementary to the method described here. Recent work has further emphasized the importance of sniff dynamics for odor identity coding and discrimination [1,[21][22][23], augmented by new analytical approaches to analyzing olfactory network dynamics, particularly the use of time warping [24,25].…”

Section: Introductionmentioning

confidence: 99%

Dynamics of odor sampling strategies in mice

et al. 2020

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Mammalian olfactory receptor neurons in the nasal cavity are stimulated by odorants carried by the inhaled air and their activation is therefore tied to and driven by the breathing or sniffing frequency. Sniffing frequency can be deliberately modulated to alter how odorants stimulate olfactory receptor neurons, giving the animal control over the frequency of odorant exposure to potentially aid odorant detection and discrimination. We monitored sniffing behaviors and odorant discrimination ability of freely-moving mice while they sampled either decreasing concentrations of target odorants or sampled a fixed target odorant concentration in the presence of a background of increasing odorant concentrations, using a Go-NoGo behavioral paradigm. This allowed us to ask how mice alter their odorant sampling duration and sampling (sniffing) frequency depending on the demands of the task and its difficulty. Mice showed an anticipatory increase in sniffing rate prior to odorant exposure and chose to sample for longer durations when exposed to odorants as compared to the solvent control odorant. Similarly, mice also took more odorant sampling sniffs when exposed to target odorants compared to the solvent control odorant. In general, odorant sampling strategies became more similar the more difficult the task was, e.g. the lower the target odorant concentration or the lower the target odorant contrast relative to the background odorant, suggesting that sniffing patterns are not preset, but are dynamically modulated by the particular task and its difficulty.

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“…For OB projection neurons, however, only little information about chemotypes is available at this point: Pcdh1 and Tbx21 (Haddad et al, 2013;Nagai et al, 2005) have been shown to be selectively expressed in a subset of OB projection neurons. CCK distinguishes a subset of TCs (superficial TCs, (Liu and Shipley, 1994;Seroogy et al, 1985;Short and Wachowiak, 2019;Sun et al, 2020); vasopressin expressing cells might constitute a further subset of superficial TCs (Lukas et al, 2019). Heterogeneous expression of both the GABAa receptor as well as voltage-gated potassium channel subunits have been observed (Padmanabhan and Urban, 2010;Panzanelli et al, 2005), albeit not linked to specific cell types.…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization of projection neuron subtypes in the mouse olfactory bulb

Zeppilli

Ackels

Attey

et al. 2020

Preprint

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Projection neurons in the mammalian olfactory bulb (OB) not only receive direct input from the nose but also directly project to diverse cortical and subcortical areas. While morphological and physiological studies have highlighted functional heterogeneity, no molecular markers have been described that could reliably delineate subtypes of projection neurons. Here, we used viral injections into olfactory cortex and fluorescent nucleus sorting to enrich OB neuronal populations for projection neurons. We then performed high-throughput single nucleus and bulk RNA deep sequencing of such enriched populations. Transcriptome analysis together with RNA in situ hybridization allowed us to identify three distinct mitral and five distinct tufted cell populations with characteristic cell adhesion and cell excitability-related gene expression patterns. Using a novel computational approach to integrate bulk and snRNA-seq data we propose that different mitral cell populations selectively project to different regions of olfactory cortex. Together, we have identified potential molecular and gene regulatory mechanisms underlying projection neuron diversity and provide critical new molecular entry points into studying the diverse functional roles of mitral and tufted cell subtypes.

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Temporal Dynamics of Inhalation-Linked Activity across Defined Subpopulations of Mouse Olfactory Bulb Neurons ImagedIn Vivo

Cited by 27 publications

References 61 publications

Respiration-Locking of Olfactory Receptor and Projection Neurons in the Mouse Olfactory Bulb and Its Modulation by Brain State

Respiration-Locking of Olfactory Receptor and Projection Neurons in the Mouse Olfactory Bulb and Its Modulation by Brain State

Dynamics of odor sampling strategies in mice

Molecular characterization of projection neuron subtypes in the mouse olfactory bulb

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