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

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.

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

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.

scholarly journals Olfactory subsystems associated with the necklace glomeruli in rodents

2020 ◽  
Author(s):  
Arthur D. Zimmerman ◽  
Steven Munger
Keyword(s):  
Olfactory Bulb ◽  
Olfactory Epithelium ◽  
Main Olfactory Bulb ◽  
Chemosensory Neurons ◽  
Main Olfactory Epithelium ◽  
Immunohistochemical Markers ◽  
Grueneberg Ganglion ◽  
Afferent Inputs ◽  
Necklace Glomeruli

The necklace glomeruli are a loosely defined group of glomeruli encircling the caudal main olfactory bulb in rodents. Initially defined by the expression of various immunohistochemical markers, they are now better understood in the context of the specialized chemosensory neurons of the main olfactory epithelium and Grueneberg ganglion that innervate them. It has become clear that the necklace region of the rodent main olfactory bulb is composed of multiple distinct groups of glomeruli, defined at least in part by their afferent inputs. In this review, we will explore the necklace glomeruli and the chemosensory neurons that innervate them.

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

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.

scholarly journals Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians

2019 ◽  
Author(s):  
Lukas Weiss ◽  
Lucas D. Jungblut ◽  
Andrea G. Pozzi ◽  
Barbara S. Zielinski ◽  
Lauren A. O’Connell ◽  
...  
Keyword(s):  
Olfactory Receptor ◽  
Olfactory Receptor Neuron ◽  
Receptor Neuron ◽  
Projection Neurons ◽  
Amphibian Species ◽  
Odor Processing ◽  
Axonal Projections ◽  
Frog Species ◽  
Receptor Neurons ◽  
Jawless Fish

Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59% and 50% connect to multiple glomeruli in larval and post-metamorphotic animals, respectively. Independent of developmental stage, lifestyle and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.Abstract Figure

scholarly journals Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size

2015 ◽  
Vol 112 (41) ◽  
pp. 12846-12851 ◽  
Author(s):  
Filomene G. Morrison ◽  
Brian G. Dias ◽  
Kerry J. Ressler
Keyword(s):  
Olfactory Bulb ◽  
Learning And Memory ◽  
Olfactory Epithelium ◽  
Olfactory System ◽  
Structural Changes ◽  
Freezing Behavior ◽  
Extinction Training ◽  
Odor Stimulus ◽  
Main Olfactory Epithelium ◽  
Odor Learning

Although much work has investigated the contribution of brain regions such as the amygdala, hippocampus, and prefrontal cortex to the processing of fear learning and memory, fewer studies have examined the role of sensory systems, in particular the olfactory system, in the detection and perception of cues involved in learning and memory. The primary sensory receptive field maps of the olfactory system are exquisitely organized and respond dynamically to cues in the environment, remaining plastic from development through adulthood. We have previously demonstrated that olfactory fear conditioning leads to increased odorant-specific receptor representation in the main olfactory epithelium and in glomeruli within the olfactory bulb. We now demonstrate that olfactory extinction training specific to the conditioned odor stimulus reverses the conditioning-associated freezing behavior and odor learning-induced structural changes in the olfactory epithelium and olfactory bulb in an odorant ligand-specific manner. These data suggest that learning-induced freezing behavior, structural alterations, and enhanced neural sensory representation can be reversed in adult mice following extinction training.

Immunocytochemical localization of the GABAB2 receptor subunit in the glomeruli of the mouse main olfactory bulb

2006 ◽  
Vol 402 (1-2) ◽  
pp. 121-125 ◽  
Author(s):  
Igor Kratskin ◽  
Natalia Kenigfest ◽  
Jean Paul Rio ◽  
Chakib Djediat ◽  
Jacques Repérant
Keyword(s):  
Olfactory Bulb ◽  
Immunocytochemical Localization ◽  
Receptor Subunit ◽  
Main Olfactory Bulb
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