A population of glomerular glutamatergic neurons controls sensory information transfer in the mouse olfactory bulb

Tatti, Roberta; Bhaukaurally, Khaleel; Gschwend, Olivier; Seal, Rebecca P.; Edwards, Robert H.; Rodríguez, Iván; Carleton, Alan

doi:10.1038/ncomms4791

Cited by 36 publications

(30 citation statements)

References 68 publications

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“…VGLUT3 is expressed in glutamatergic, GABAergic (Fremeau et al, ), cholinergic (Gras et al, ), and serotonergic neurons (Hioki et al, ) in many parts of the nervous system. The staining pattern in the mouse OB was similar to that previously reported (Tatti et al, ).…”

Section: Methodssupporting

confidence: 90%

Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb

Hamamoto

Kiyokage

Sohn

et al. 2016

J of Comparative Neurology

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Odor information is regulated by olfactory inputs, bulbar interneurons, and centrifugal inputs in the olfactory bulb (OB). Cholinergic neurons projecting from the nucleus of the horizontal limb of the diagonal band of Broca and the magnocellular preoptic nucleus are one of the primary centrifugal inputs to the OB. In this study, we focused on cholinergic regulation of the OB and analyzed neural morphology with a particular emphasis on the projection pathways of cholinergic neurons. Single-cell imaging of a specific neuron within dense fibers is critical to evaluate the structure and function of the neural circuits. We labeled cholinergic neurons by infection with virus vector and then reconstructed them three-dimensionally. We also examined the ultramicrostructure of synapses by electron microscopy tomography. To further clarify the function of cholinergic neurons, we performed confocal laser scanning microscopy to investigate whether other neurotransmitters are present within cholinergic axons in the OB. Our results showed the first visualization of complete cholinergic neurons, including axons projecting to the OB, and also revealed frequent axonal branching within the OB where it innervated multiple glomeruli in different areas. Furthermore, electron tomography demonstrated that cholinergic axons formed asymmetrical synapses with a morphological variety of thicknesses of the postsynaptic density. Although we have not yet detected the presence of other neurotransmitters, the range of synaptic morphology suggests multiple modes of transmission. The present study elucidates the ways that cholinergic neurons could contribute to the elaborate mechanisms involved in olfactory processing in the OB. J. Comp. Neurol. 525:574-591, 2017. © 2016 Wiley Periodicals, Inc.

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Section: Methodssupporting

confidence: 90%

Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb

Hamamoto

Kiyokage

Sohn

et al. 2016

J of Comparative Neurology

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“…These cells match the known characteristics of SA cells (Aungst et al, 2003; Borisovska et al, 2013; Chand et al, 2015; Kiyokage et al, 2010; Kosaka and Kosaka, 2011; Liu et al, 2013; Tatti et al, 2014; Wachowiak et al, 2013; Whitesell et al, 2013). We asked two questions in this study.…”

Section: Introductionsupporting

confidence: 60%

An Interglomerular Circuit Gates Glomerular Output and Implements Gain Control in the Mouse Olfactory Bulb

Banerjee

Marbach

Anselmi

et al. 2015

Neuron

151

194

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Summary Odors elicit distributed activation of glomeruli in the olfactory bulb (OB). Crosstalk between co-active glomeruli has been proposed to perform a variety of computations, facilitating efficient extraction of sensory information by the cortex. Dopaminergic/GABAergic cells in the OB, which can be identified by their expression of the dopamine transporter (DAT), provide the earliest opportunity for such crosstalk. Here we show in mice that DAT+ cells carry concentration dependent odor signals and broadcast focal glomerular inputs throughout the OB to cause suppression of mitral/tufted (M/T) cell firing, an effect that is mediated by the external tufted (ET) cells coupled to DAT+ cells via chemical and electrical synapses. We find that DAT+ cells implement gain control and decorrelate odor representations in the M/T cell population. Our results further indicate that ET cells are gatekeepers of glomerular output and prime determinants of M/T responsiveness.

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“…These concentrations have previously been shown to activate dense glomeruli patterns (see for quantifications14). We performed tetrode recordings in the olfactory bulb of awake head-restrained mice9111718 exposed to natural odorants, and isolated individual M/T cells ( n = 81 M/T cells from 4 mice). As previously described9, M/T cells responded to the stimuli with weak and phasic firing rate changes, as observed on the peristimulus time histograms (50 ms binned PSTH; Fig.…”

Section: Resultsmentioning

confidence: 99%

Dense encoding of natural odorants by ensembles of sparsely activated neurons in the olfactory bulb

Gschwend

Beroud

Vincis

et al. 2016

Sci Rep

Self Cite

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Sensory information undergoes substantial transformation along sensory pathways, usually encompassing sparsening of activity. In the olfactory bulb, though natural odorants evoke dense glomerular input maps, mitral and tufted (M/T) cells tuning is considered to be sparse because of highly odor-specific firing rate change. However, experiments used to draw this conclusion were either based on recordings performed in anesthetized preparations or used monomolecular odorants presented at arbitrary concentrations. In this study, we evaluated the lifetime and population sparseness evoked by natural odorants by capturing spike temporal patterning of neuronal assemblies instead of individual M/T tonic activity. Using functional imaging and tetrode recordings in awake mice, we show that natural odorants at their native concentrations are encoded by broad assemblies of M/T cells. While reducing odorant concentrations, we observed a reduced number of activated glomeruli representations and consequently a narrowing of M/T tuning curves. We conclude that natural odorants at their native concentrations recruit M/T cells with phasic rather than tonic activity. When encoding odorants in assemblies, M/T cells carry information about a vast number of odorants (lifetime sparseness). In addition, each natural odorant activates a broad M/T cell assembly (population sparseness).

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A population of glomerular glutamatergic neurons controls sensory information transfer in the mouse olfactory bulb

Cited by 36 publications

References 68 publications

Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb

Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb

An Interglomerular Circuit Gates Glomerular Output and Implements Gain Control in the Mouse Olfactory Bulb

Dense encoding of natural odorants by ensembles of sparsely activated neurons in the olfactory bulb

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