Widespread Inhibition, Antagonism, and Synergy in Mouse Olfactory Sensory Neurons In Vivo

Inagaki, Shinji; Iwata, Ren; Iwamoto, Masakazu; Imai, Takeshi

doi:10.1016/j.celrep.2020.107814

Cited by 59 publications

(67 citation statements)

References 61 publications

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“…Beyond our theoretical observations, there are other more recent experimental studies that report related effects [18][19][20] . Our work is unique in the following regard: (1) we report responses from a large set of OSNs in intact, freely breathing mice, responding to vapor phase odorants inhaled physiologically, (2) we report fast, real-time responses with a variety of odorants and using both OSN and glomerular imaging and (3) we report responses to mixtures of high complexity (up to 12 odors), well beyond just binary mixtures.…”

Section: Discussionmentioning

confidence: 53%

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Antagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice

et al. 2020

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Odor landscapes contain complex blends of molecules that each activate unique, overlapping populations of olfactory sensory neurons (OSNs). Despite the presence of hundreds of OSN subtypes in many animals, the overlapping nature of odor inputs may lead to saturation of neural responses at the early stages of stimulus encoding. Information loss due to saturation could be mitigated by normalizing mechanisms such as antagonism at the level of receptorligand interactions, whose existence and prevalence remains uncertain. By imaging OSN axon terminals in olfactory bulb glomeruli as well as OSN cell bodies within the olfactory epithelium in freely breathing mice, we find widespread antagonistic interactions in binary odor mixtures. In complex mixtures of up to 12 odorants, antagonistic interactions are stronger and more prevalent with increasing mixture complexity. Therefore, antagonism is a common feature of odor mixture encoding in OSNs and helps in normalizing activity to reduce saturation and increase information transfer.

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Section: Discussionmentioning

confidence: 53%

“…1b, c). Experimental work in vitro in OSNs has suggested the existence of nonlinear interactions, especially antagonism or partial antagonism [12][13][14][15][16][17][18][19][20] . However, the prevalence of these interactions, especially in living animals within the constraints of natural sniffing dynamics, has not been explored.…”

mentioning

confidence: 99%

Antagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice

et al. 2020

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“…This reduction could be could be due to adaptation of OSN inputs 48 , inhibition at the receptor level 60,61 , or inhibition of ongoing glutamatergic drive from ET cells 11,12 . Overall, the high correspondence between glutamatergic input and MT cell output patterns suggests that transformations of odor representations by OB circuitry-at least in the spatial and temporal domains -may be more limited than previously thought.…”

Section: Multisynaptic Glutamatergic Excitation May Preferentially Drmentioning

confidence: 99%

Diverse dynamics of glutamatergic input from sensory neurons underlie heterogeneous responses of olfactory bulb outputs in vivo

Eiting

Wachowiak

2019

Preprint

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Mitral/tufted (MT) cells of the olfactory bulb (OB) show diverse temporal responses to odorant stimulation that are thought to encode odor information. To understand the role of sensory input dynamics versus OB circuit mechanisms in generating this diversity, we imaged glutamate signaling onto MT cell dendrites in anesthetized and awake mice. We found surprising diversity in the dynamics of these signals, including excitatory, suppressive, and biphasic responses as well as nonlinear changes in glutamate over multiple inhalations. Glutamate response patterns persisted after blockade of postsynaptic activity, implicating sensory neurons as the primary source of glutamate signaling onto MT cells. Simultaneous imaging of glutamate and calcium signals from MT cell dendrites revealed highly correlated responses for both signals. Thus, the dynamics of sensory input alone, rather than emergent features of OB circuits, may account for much of the diversity in MT cell responses that underlies odor representations at this stage.

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“…Here, the synergistic effects were seen preferentially for low concentrations of odorants in the mix. In comparison, antagonism was predominant for higher concentrations of odorants in the mixture (Inagaki, et al, 2020). These synergistic effects could indicate an allosteric mechanism, even though this type of modulation has rarely been reported for Class A GPCRs.…”

Section: Odor Mixtures and Odorant-or Interactions In The Oementioning

confidence: 83%

“…These experiments now shed a markedly new light on explanations of odor coding at the peripheral level. Specifically, results show that peripheral odor coding involves odorants acting on receptors as agonists, antagonists, inverse agonists, partial agonists, and even have a synergistic effect (de March, et al, 2020, Inagaki, et al, 2020, McClintock, et al, 2020, Pfister, et al, 2020, Reddy, et al, 2018, Xu, et al, 2020, Zak, et al, 2020.…”

Section: Odor Mixtures and Odorant-or Interactions In The Oementioning

confidence: 99%

Odor Coding in the Mammalian Olfactory Epithelium

Kurian¹,

Naressi²,

Manoel³

et al. 2020

Preprint

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Noses are extremely sophisticated chemical detectors allowing animals to use scents to interpret and navigate their environments. Odor detection starts with the activation of odorant receptors (ORs), expressed in mature olfactory sensory neurons (OSNs) populating the olfactory mucosa. Different odorants, or different concentrations of the same odorant, activate unique ensembles of ORs. This mechanism of combinatorial receptor coding provided a possible explanation as to why different odorants are perceived as having distinct odors. Aided by new technologies, several recent studies have found that antagonist interactions also play an important role in the formation of the combinatorial receptor code. These findings mark the start of a new era in the study of odorant-receptor interactions and add a new level of complexity to odor coding in mammals.

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Widespread Inhibition, Antagonism, and Synergy in Mouse Olfactory Sensory Neurons In Vivo

Cited by 59 publications

References 61 publications

Antagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice

Antagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice

Diverse dynamics of glutamatergic input from sensory neurons underlie heterogeneous responses of olfactory bulb outputs in vivo

Odor Coding in the Mammalian Olfactory Epithelium

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