Faculty Opinions recommendation of Principles of glomerular organization in the human olfactory bulb--implications for odor processing.

AbstractOlfactory dysfunction is a prevalent non-motor symptom of Parkinson’s disease (PD). This dysfunction is a result of neurodegeneration within the olfactory bulb (OB), the first processing area of the central olfactory system, and commonly precedes the characteristic motor symptoms in PD by several years. Functional measurements of the OB could therefore potentially be used as an early biomarker for PD. Here, we used a non-invasive method, so-called electrobulbogram (EBG), to measure OB function in PD and age-matched healthy controls to assess whether EBG measures can dissociate PDs from controls. We estimated the spectrogram of the EBG signal during exposure to odor in PD (n = 20) and age-matched controls (n = 18) as well as identified differentiating patterns of odor-related synchronization in the gamma, beta, and theta frequency bands. Moreover, we assessed if these PD-EBG components could dissociate PD from control as well as their relationship with PD characteristics. We identified six EBG components during the initial and later stages of odor processing which dissociated PD from controls with 90% sensitivity and 100% specificity with links to PD characteristics. These PD-EBG components were related to medication, disease duration, and severity, as well as clinical odor identification performance. These findings support using EBG as a tool to experimentally assess PD interventions, potentially aid diagnosis, and the potential development of EBG into an early biomarker for PD.

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Immature olfactory sensory neurons provide behaviorally useful sensory input to the olfactory bulb

10.1101/2021.01.06.425578 ◽

2021 ◽

Author(s):

Jane S Huang ◽

Tenzin Kunkhyen ◽

Beichen Liu ◽

Ryan J Muggleton ◽

Jonathan T Avon ◽

...

Keyword(s):

Olfactory Bulb ◽

Sensory Neurons ◽

Sensory Input ◽

Odorant Receptors ◽

Projection Neurons ◽

Olfactory Sensory Neurons ◽

Odor Processing ◽

Newborn Neurons ◽

Behavioral Assays

Postnatal neurogenesis provides an opportunity to understand how newborn neurons functionally integrate into circuits to restore lost function. Newborn olfactory sensory neurons (OSNs) wire into highly organized olfactory bulb (OB) circuits throughout life, enabling lifelong plasticity and regeneration. Immature OSNs can form functional synapses capable of evoking firing in OB projection neurons. However, what contribution, if any, immature OSNs make to odor processing is unknown. Indeed, because immature OSNs can express multiple odorant receptors, any input that they do provide could degrade the odorant selectivity of input to OB glomeruli. Here, we used a combination of in vivo 2-photon calcium imaging, optogenetics, electrophysiology and behavioral assays to show that immature OSNs provide odor input to the OB, where they form monosynaptic connections with excitatory neurons. Importantly, immature OSNs responded as selectively to odorants as mature OSNs. Furthermore, mice successfully performed odor detection tasks using sensory input from immature OSNs alone. Immature OSNs responded more strongly to low odorant concentrations but their responses were less concentration dependent than those of mature OSNs, suggesting that immature and mature OSNs provide distinct odor input streams to each glomerulus. Together, our findings suggest that sensory input mediated by immature OSNs plays a previously unappreciated role in olfactory-guided behavior.

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Both Electrical and Chemical Synapses Mediate Fast Network Oscillations in the Olfactory Bulb

Journal of Neurophysiology ◽

10.1152/jn.00887.2002 ◽

2003 ◽

Vol 89 (5) ◽

pp. 2601-2610 ◽

Cited By ~ 73

Author(s):

Daniel Friedman ◽

Ben W. Strowbridge

Keyword(s):

Olfactory Bulb ◽

Molecular Mechanisms ◽

Cell Activity ◽

Cellular Mechanisms ◽

Odor Processing ◽

Network Oscillations ◽

Fast Network ◽

Fast Oscillations

Odor perception depends on a constellation of molecular, cellular, and network interactions in olfactory brain areas. Recently, there has been better understanding of the cellular and molecular mechanisms underlying the odor responses of neurons in the olfactory epithelium, the first-order olfactory area. In higher order sensory areas, synchronized activity in networks of neurons is known to be a prominent feature of odor processing. The perception and discrimination of odorants is associated with fast (20–70 Hz) electroencephalographic oscillations. The cellular mechanisms underlying these fast network oscillations have not been defined. In this study, we show that synchronous fast oscillations can be evoked by brief electrical stimulation in the rat olfactory bulb in vitro, partially mimicking the natural response of this brain region to sensory input. Stimulation induces periodic inhibitory synaptic potentials in mitral cells and prolonged spiking in GABAergic granule cells. Repeated stimulation leads to the persistent enhancement in both granule cell activity and mitral cell inhibition. Prominent oscillations in field recordings indicate that stimulation induces high-frequency activity throughout networks of olfactory bulb neurons. Network synchronization results from chemical and electrical synaptic interactions since both glutamate-receptor antagonists and gap junction inhibitors block oscillatory intracellular and field responses. Our results demonstrate that the olfactory bulb can generate fast oscillations autonomously through the persistent activation of networks of inhibitory interneurons. These local circuit interactions may be critically involved in odor processing in vivo.

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Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb.

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.90.8.3329 ◽

1993 ◽

Vol 90 (8) ◽

pp. 3329-3333 ◽

Cited By ~ 167

Author(s):

K. M. Guthrie ◽

A. J. Anderson ◽

M. Leon ◽

C. Gall

Keyword(s):

Olfactory Bulb ◽

Mrna Expression ◽

Odor Processing

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Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

Cell and Tissue Research ◽

10.1007/s00441-021-03527-3 ◽

2021 ◽

Author(s):

Lukas Weiss ◽

Paola Segoviano Arias ◽

Thomas Offner ◽

Sara Joy Hawkins ◽

Thomas Hassenklöver ◽

...

Keyword(s):

Olfactory Bulb ◽

Xenopus Laevis ◽

Water System ◽

Projection Neurons ◽

Main Olfactory Bulb ◽

Behavioral Experiments ◽

Main Olfactory Epithelium ◽

Odor Processing ◽

Interhemispheric Connectivity ◽

Receptor Neurons

AbstractDuring metamorphosis, the olfactory system of anuran tadpoles undergoes substantial restructuring. The main olfactory epithelium in the principal nasal cavity of Xenopus laevis tadpoles is associated with aquatic olfaction and transformed into the adult air-nose, while a new adult water-nose emerges in the middle cavity. Impacts of this metamorphic remodeling on odor processing, behavior, and network structure are still unexplored. Here, we used neuronal tracings, calcium imaging, and behavioral experiments to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity project axons to glomeruli in the ventral main olfactory bulb. These projections are gradually replaced by receptor neuron axons from the newly forming middle cavity epithelium. Despite this reorganization in the ventral bulb, two spatially segregated odor processing streams remain undisrupted and behavioral responses to waterborne odorants are unchanged. Contemporaneously, new receptor neurons in the remodeling principal cavity innervate the emerging dorsal part of the bulb, which displays distinct wiring features. Glomeruli around its midline are innervated from the left and right nasal epithelia. Additionally, postsynaptic projection neurons in the dorsal bulb predominantly connect to multiple glomeruli, while half of projection neurons in the ventral bulb are uni-glomerular. Our results show that the “water system” remains functional despite metamorphic reconstruction. The network differences between the dorsal and ventral olfactory bulb imply a higher degree of odor integration in the dorsal main olfactory bulb. This is possibly connected with the processing of different odorants, airborne vs. waterborne.

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Distinct interhemispheric connectivity at the level of the olfactory bulb emerges during Xenopus laevis metamorphosis

10.1101/2021.05.11.443461 ◽

2021 ◽

Author(s):

Lukas Weiss ◽

Paola Segoviano Arias ◽

Thomas Offner ◽

Sara Joy Hawkins ◽

Thomas Hassenkloever ◽

...

Keyword(s):

Olfactory Bulb ◽

Xenopus Laevis ◽

Water System ◽

Projection Neurons ◽

Main Olfactory Bulb ◽

Epithelial Surface ◽

Main Olfactory Epithelium ◽

Odor Processing ◽

Interhemispheric Connectivity ◽

Receptor Neurons

The olfactory system of anuran tadpoles requires substantial restructuring to adapt to the lifestyle of the adult frogs. Xenopus laevis tadpoles have a single main olfactory epithelium in the principal nasal cavity associated with aquatic olfaction. After metamorphosis, this epithelial surface is transformed into the adult air-nose and a new epithelium, the adult water-nose, is present in the middle cavity. Impacts of this massive remodeling on odor processing, behavior and network structure are still unexplored. In the present study, we used neuronal tracings, calcium imaging and a behavioral assay to examine the functional connectivity between the epithelium and the main olfactory bulb during metamorphosis. In tadpoles, olfactory receptor neurons in the principal cavity epithelium project axons to glomeruli in the ventral main olfactory bulb. During metamorphosis, these projections are gradually replaced by receptor neuron axons emerging from the newly forming middle cavity epithelium. Despite this metamorphotic reorganization in the ventral bulb, two spatially and functionally segregated odor processing streams remain undisrupted. In line with this, metamorphotic rewiring does not alter behavioral responses to waterborne odorants. Contemporaneously, newly formed receptor neurons in the remodeling principal cavity epithelium project their axons to the dorsal part of the bulb. The emerging neuronal networks of the dorsal and ventral main olfactory bulb show substantial differences. Glomeruli around the midline of the dorsal bulb are innervated from the left and right nasal epithelia. In addition, postsynaptic projection neurons in the dorsal bulb predominantly have smaller tufts and connect to multiple glomeruli, while more than half of projection neurons in the ventral bulb have a single, bigger tuft. Our results show that during the metamorphotic reconstruction of the olfactory network the water system remains functional. Differences of the neuronal network of the dorsal and ventral olfactory bulb imply that a higher degree of odor integration takes place in the dorsal main olfactory bulb. This is likely connected with the processing of different odorants, airborne vs. waterborne, in these two parts of the olfactory bulb.

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