Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Huang, Jane S.; Kunkhyen, Tenzin; Rangel, Alexander N.; Brechbill, Taryn R.; Gregory, Jordan; Winson-Bushby, Emily D.; Liu, Beichen; Avon, Jonathan T.; Muggleton, Ryan J.; Cheetham, Claire E. J.

doi:10.1038/s41467-022-33967-6

Cited by 19 publications

(16 citation statements)

References 108 publications

(206 reference statements)

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“…The data that support the findings of this study are available in Zenodo with the identifier https://doi.org/10.5281/zenodo.7013681 102 . The data for relevant figure panels in Fig.…”

Section: Data Availabilitysupporting

confidence: 71%

Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Huang

Kunkhyen

Liu

et al. 2021

Preprint

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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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“…The data that support the findings of this study are available in Zenodo with the identifier https://doi.org/10.5281/zenodo.7013681 102 . The data for relevant figure panels in Fig.…”

Section: Data Availabilitysupporting

confidence: 71%

Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Huang

Kunkhyen

Liu

et al. 2021

Preprint

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“…It may therefore be hypothesized that the impact of both ARL13B and AC3 on maturation was a result of sensory deprivation. Additionally, the crucial process of synaptogenesis occurs during OSN maturation and recently the exuberant and plastic nature of the iOSN synapse has been revealed ( Cheetham et al, 2016 ; Huang et al, 2022 ; Marcucci et al, 2011 ). Perhaps both peripheral odorant detection and the subsequent synaptic transmission are necessary for the maturation of an OSN.…”

Section: Discussionmentioning

confidence: 99%

The role of a ciliary GTPase in the regulation of neuronal maturation of olfactory sensory neurons

et al. 2023

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Olfactory sensory neurons (OSNs) form embryonically and mature perinatally, innervating glomeruli and extending dendrites with multiple cilia. This process and its timing are crucial for odor detection and perception and continues throughout life. In the olfactory epithelium (OE), differentiated OSNs proceed from an immature (iOSN) to a mature (mOSN) state through well-defined sequential morphological and molecular transitions, but the precise mechanisms controlling OSN maturation remain largely unknown. We have identified that a GTPase, ARL13B, has a transient and maturation state-dependent expression in OSNs marking the emergence of a primary cilium. Utilizing an iOSN-specific Arl13b-null murine model, we examined the role of ARL13B in the maturation of OSNs. The loss of Arl13b in iOSNs caused a profound dysregulation of the cellular homeostasis and development of the OE. Importantly, Arl13b null OSNs demonstrated a delay in the timing of their maturation. Finally, the loss of Arl13b resulted in severe deformation in the structure and innervation of glomeruli. Our findings demonstrate a previously unknown role of ARL13B in the maturation of OSNs and development of the OE.

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“…In adult humans, the number of newly formed neurons in the OB is significantly lower compared to rodents. However, there is some evidence indicating that new neurons are continuously incorporated in the human OB during adulthood [ 38 , 39 ]. Therefore, the dysfunction of adult neurogenesis in the OB may contributes to the olfactory symptoms occurring in AD.…”

Section: Discussionmentioning

confidence: 99%

Dimethyl Fumarate Alleviates Adult Neurogenesis Disruption in Hippocampus and Olfactory Bulb and Spatial Cognitive Deficits Induced by Intracerebroventricular Streptozotocin Injection in Young and Aged Rats

Kurowska

Ruciński

Myślińska

et al. 2022

IJMS

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The disorder of adult neurogenesis is considered an important mechanism underlying the learning and memory impairment observed in Alzheimer’s disease (AD). The sporadic nonhereditary form of AD (sAD) affects over 95% of AD patients and is related to interactions between genetic and environmental factors. An intracerebroventricular injection of streptozotocin (STZ-ICV) is a representative and well-established method to induce sAD-like pathology. Dimethyl fumarate (DMF) has antioxidant and anti-inflammatory properties and is used for multiple sclerosis treatment. The present study determines whether a 26-day DMF therapy ameliorates the disruption of adult neurogenesis and BDNF-related neuroprotection in the hippocampus and olfactory bulb (OB) in an STZ-ICV rat model of sAD. Considering age as an important risk factor for developing AD, this study was performed using 3-month-old (the young group) and 22-month-old (the aged group) male Wistar rats. Spatial cognitive functions were evaluated with the Morris water maze task. Immunofluorescent labelling was used to assess the parameters of adult neurogenesis and BDNF-related neuroprotection in the hippocampus and OB. Our results showed that the STZ-ICV evoked spatial learning and memory impairment and disturbances in adult neurogenesis and BDNF expression in both examined brain structures. In the aged animals, the deficits were more severe. We found that the DMF treatment significantly alleviated STZ-ICV-induced behavioural and neuronal disorders in both age groups of the rats. Our findings suggest that DMF, due to its beneficial effect on the formation of new neurons and BDNF-related neuroprotection, may be considered as a promising new therapeutic agent in human sAD.

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Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Cited by 19 publications

References 108 publications

Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

The role of a ciliary GTPase in the regulation of neuronal maturation of olfactory sensory neurons

Dimethyl Fumarate Alleviates Adult Neurogenesis Disruption in Hippocampus and Olfactory Bulb and Spatial Cognitive Deficits Induced by Intracerebroventricular Streptozotocin Injection in Young and Aged Rats

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