Elsevier

Neuroscience

Volume 170, Issue 3, 27 October 2010, Pages 881-892
Neuroscience

Pain Mechanisms and Sensory Neuroscience
Research Paper
Integration of CO2 and odorant signals in the mouse olfactory bulb

https://doi.org/10.1016/j.neuroscience.2010.08.006Get rights and content

Abstract

Carbon dioxide (CO2) is an important environmental cue for many animal species. In both vertebrates and invertebrates, CO2 is detected by a specialized subset of olfactory sensory neurons (OSNs) and mediates several stereotypical behaviors. It remains unknown how CO2 cues are integrated with other olfactory signals in the mammalian olfactory bulb, the first stage of central olfactory processing. By recording from the mouse olfactory bulb in vivo, we found that CO2-activating neurons also respond selectively to odorants, many of which are putative mouse pheromones and natural odorants. In addition, many odorant-responsive bulbar neurons are inhibited by CO2. For a substantial number of CO2-activating neurons, binary mixtures of CO2 and a specific odorant produce responses that are distinct from those evoked by either CO2 or the odorant alone. In addition, for a substantial number of CO2-inhibiting neurons, CO2 addition can completely block the action potential firing of the cells to the odorants. These results indicate strong interaction between CO2 signals and odorant signals in the olfactory bulb, suggesting important roles for the integration of these two signals in CO2-mediated behavioral responses.

Section snippets

Animals and anesthesia

Animal care and use conformed to the institutional guidelines of the National Institute of Biological Science and were in accordance with the policies of the US National Institute of Health. Male C57/BL6 mice (8–12 weeks) were obtained from VitalRiver Laboratory Animal Inc. (Beijing, China). For anesthesia, mice were injected with atropine (50 mg/kg, i.p., Sigma-Aldrich) and then urethane (1.64 g/kg, i.p., Sinopharm, Shanghai, China).

Electrophysiology

After anesthesia, a mouse was placed on a custom-made

CO2-activating neurons in the olfactory bulb respond selectively to odorants

To test whether bulbar neurons can respond to both CO2 and odorants, we first searched for CO2-activating neurons by targeting recording electrodes into the caudal end of the olfactory bulb where the necklace glomeruli are located (Hu et al., 2007, Walz et al., 2007). Putative M/T cells were identified based on the fact that these cells were recorded from a thin layer with clear spontaneous activity coupled to respiratory rhythms. CO2-responsiveness was tested by puffing 2-s CO2 pulses

Discussion

In mice, CO2 activates a specialized subset of OSNs that project to the necklace glomeruli in the caudal olfactory bulb (Hu et al., 2007, Sun et al., 2009). Our recordings from this study revealed that CO2-activating bulbar neurons also respond to odorants, suggesting strong interaction between CO2 and odorant signals in the olfactory bulb. Here we will discuss the implications of our data on the function of CO2 as a behavioral cue as well as the possible circuitry mechanisms underlying the

Acknowledgments

We thank A.L. Person for critical reading of the manuscript. This study was supported by a Project 973 grant (2010CB833902) and a Project 863 grant (2008AA022312) from China Ministry of Science and Technology to ML.

References (30)

  • E.A. Hallem et al.

    Acute carbon dioxide avoidance in Caenorhabditis elegans

    Proc Natl Acad Sci U S A

    (2008)
  • J. Hu et al.

    Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse

    Science

    (2007)
  • W.D. Jones et al.

    Two chemosensory receptors together mediate carbon dioxide detection in Drosophila

    Nature

    (2007)
  • D.M. Juilfs et al.

    A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway

    Proc Natl Acad Sci U S A

    (1997)
  • L.M. Kay et al.

    A redefinition of odor mixture quality

    Behav Neurosci

    (2005)
  • Cited by (0)

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