Mouse Grueneberg ganglion neurons share molecular and functional features with C. elegans amphid neurons

Brechbühl, Julien; Moine, Fabian; Broillet, Marie-Christine

doi:10.3389/fnbeh.2013.00193

Cited by 23 publications

(44 citation statements)

References 84 publications

(162 reference statements)

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“…In other species, specifically in rodents, the niche of thermosensors lies in the GG (Mamasuew et al, 2008;Brechbühl et al, 2014). This organ is quite distinct from the main olfactory epithelium, and the axons of GG neurons project to the necklace glomeruli of the olfactory bulb (Fuss et al, 2005).…”

Section: Afferent Innervation Pattern Of the ␥-Glomerulusmentioning

confidence: 99%

“…These cells show a graded and temperature-dependent Ca 2ϩ influx at their somata (Schmid et al, 2010), and their axons project to the so-called necklace glomeruli in the olfactory bulb (Fuss et al, 2005;Koos and Fraser, 2005;Fleischer et al, 2006;Roppolo et al, 2006;Storan and Key, 2006). The temperature-sensing transduction mechanisms in these neurons via a cGMP-mediated cascade have been characterized lately in mice and in other rodents Brechbühl et al, 2014;Chao et al, 2015). Thermosensitivity thus appears not to be restricted to the Grueneberg system of the mouse.…”

Section: Introductionmentioning

confidence: 99%

“…Neurons of the Grueneberg ganglion (GG) of the mouse were shown to respond to chemosensory cues, including alarm pheromones as well as cool ambient temperatures (Brechbühl et al, 2008(Brechbühl et al, , 2013Mamasuew et al, 2008Mamasuew et al, , 2011Hanke et al, 2013). These cells show a graded and temperature-dependent Ca 2ϩ influx at their somata (Schmid et al, 2010), and their axons project to the so-called necklace glomeruli in the olfactory bulb (Fuss et al, 2005;Koos and Fraser, 2005;Fleischer et al, 2006;Roppolo et al, 2006;Storan and Key, 2006).…”

Section: Introductionmentioning

confidence: 99%

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Integrating Temperature with Odor Processing in the Olfactory Bulb

et al. 2015

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Temperature perception has long been classified as a somesthetic function solely. However, in recent years several studies brought evidence that temperature perception also takes place in the olfactory system of rodents. Temperature has been described as an effective stimulus for sensory neurons of the Grueneberg ganglion located at the entrance of the nose. Here, we investigate whether a neuronal trace of temperature stimulation can be observed in the glomeruli and mitral cells of the olfactory bulb, using calcium imaging and fast line-scanning microscopy. We show in the Xenopus tadpole system that the ␥-glomerulus, which receives input from olfactory neurons, is highly sensitive to temperature drops at the olfactory epithelium. We observed that thermo-induced activity in the ␥-glomerulus is conveyed to the mitral cells innervating this specific neuropil. Surprisingly, a substantial number of thermosensitive mitral cells were also chemosensitive. Moreover, we report another unique feature of the ␥-glomerulus: it receives ipsilateral and contralateral afferents. The latter fibers pass through the contralateral bulb, cross the anterior commissure, and then run to the ipsilateral olfactory bulb, where they target the ␥-glomerulus. Temperature drops at the contralateral olfactory epithelium also induced responses in the ␥-glomerulus and in mitral cells. Temperature thus appears to be a relevant physiological input to the Xenopus olfactory system. Each olfactory bulb integrates and codes temperature signals originating from receptor neurons of the ipsilateral and contralateral nasal cavities. Finally, temperature and chemical information is processed in shared cellular networks.

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Section: Afferent Innervation Pattern Of the ␥-Glomerulusmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Integrating Temperature with Odor Processing in the Olfactory Bulb

et al. 2015

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“…Finally in mice the Grueneberg ganglion located at the tip of the nose close to the entry of the naris, has been identified as a chemodetector of alarm pheromones. Brechbühl et al (2013) investigated the conserved multisensory modalities of mouse Grueneberg ganglion neurons. They found striking similarities between mouse Grueneberg ganglion neurons and nematode amphid neurons, suggesting that the ability of an organism to detect cues from similar origin occurs in a cluster of specialized olfactory neurons that has been conserved throughout evolution.…”

Section: Behavioral Neurosciencementioning

confidence: 99%

Olfactory memory networks: from emotional learning to social behaviors

2015

Frontiers Research Topics

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Odors are powerful stimuli that can evoke emotional states, and support learning and memory. Decades of research have indicated that the neural basis for this strong "odor-emotional memory" connection is due to the uniqueness of the anatomy of the olfactory pathways. Indeed, unlike the other sensory systems, the sense of smell does not pass through the thalamus to be routed to the cortex. Rather, odor information is relayed directly to the limbic system, a brain region typically associated with memory and emotional processes. This provides olfaction with a unique and potent power to influence mood, acquisition of new information, and use of information in many different contexts including social interactions. Indeed, olfaction is crucially involved in behaviors essential for survival of the individual and species, including identification of predators, recognition of individuals for procreation or social hierarchy, location of food, as well as attachment between mating pairs and infant-caretaker dyads. Importantly, odors are sampled through sniffing behavior. This active sensing plays an important role in exploratory behaviors observed in the different contexts mentioned above. Odors are also critical for learning and memory about events and places and constitute efficient retrieval cues for the recall of emotional episodic memories.This broad role for odors appears highly preserved across species. In addition, the consistent early developmental emergence of olfactory function across diverse species also provides a unique window of opportunity for analysis of myriad behavioral systems from rodents to nonhuman primates and humans. This, when combined with the relatively conserved organization of the olfactory system in mammals, provides a powerful framework to explore how complex behaviors can be modulated by odors to produce adaptive responses, and to investigate the underlying neural networks.The present research topic brings together cutting edge research on diverse species and developmental stages, highlighting convergence and divergence between humans and animals to facilitate translational research. It is composed of 25 articles and encompasses 5 sections: human olfaction, odor preferences and aversions, odors and social behavior, olfaction and sniffing, and olfactory memory. Pazart et al. (2014) designed an fMRI study to describe the differences in brain activation in wine experts compared to control subjects. They observed specific areas activated in the experts' brains during all phases of wine tasting and reported that wine experts showed a more immediate and targeted sensory reaction to wine stimulation than control subjects. Saive et al. (2014a) reviewed and discussed the different ways of investigating episodic memory in human, ranging from autobiographical approaches to laboratory-based approaches including more ecological paradigms. In an accompanying article, Saive et al. (2014b) presented a novel laboratory-based approach to study episodic memory, which led to the formation and subsequent retriev...

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“…In rodents, the main olfactory bulb receives input from the Grueneberg ganglion (GG), an organ in the nasal cavity, consisting of thermosensitive neurons. GG neurons respond to cool temperatures 1 as well as to chemical stimuli, and their chemosensitivity is modulated by temperature fluctuations 2 . These observations suggest that the olfactory bulb may integrate chemical and temperature information collected at the nose.…”

Section: Introductionmentioning

confidence: 99%

Recording Temperature-induced Neuronal Activity through Monitoring Calcium Changes in the Olfactory Bulb of <em>Xenopus laevis</em>

Brinkmann

Okom

Kludt

et al. 2016

JoVE

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The olfactory system, specialized in the detection, integration and processing of chemical molecules is likely the most thoroughly studied sensory system. However, there is piling evidence that olfaction is not solely limited to chemical sensitivity, but also includes temperature sensitivity. Premetamorphic Xenopus laevis are translucent animals, with protruding nasal cavities deprived of the cribriform plate separating the nose and the olfactory bulb. These characteristics make them well suited for studying olfaction, and particularly thermosensitivity. The present article describes the complete procedure for measuring temperature responses in the olfactory bulb of X. laevis larvae. Firstly, the electroporation of olfactory receptor neurons (ORNs) is performed with spectrally distinct dyes loaded into the nasal cavities in order to stain their axon terminals in the bulbar neuropil. The differential staining between left and right receptor neurons serves to identify the γ-glomerulus as the only structure innervated by contralateral presynaptic afferents. Secondly, the electroporation is combined with focal bolus loading in the olfactory bulb in order to stain mitral cells and their dendrites. The 3D brain volume is then scanned under line-illumination microscopy for the acquisition of fast calcium imaging data while small temperature drops are induced at the olfactory epithelium. Lastly, the post-acquisition analysis allows the morphological reconstruction of the thermosensitive network comprising the γ-glomerulus and its innervating mitral cells, based on specific temperatureinduced Ca 2+ traces. Using chemical odorants as stimuli in addition to temperature jumps enables the comparison between thermosensitive and chemosensitive networks in the olfactory bulb.

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Mouse Grueneberg ganglion neurons share molecular and functional features with C. elegans amphid neurons

Cited by 23 publications

References 84 publications

Integrating Temperature with Odor Processing in the Olfactory Bulb

Integrating Temperature with Odor Processing in the Olfactory Bulb

Olfactory memory networks: from emotional learning to social behaviors

Recording Temperature-induced Neuronal Activity through Monitoring Calcium Changes in the Olfactory Bulb of <em>Xenopus laevis</em>

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