Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors
Open accessAbstract
Most sensory systems are primarily specialized to detect one sensory modality. Here we report that olfactory sensory neurons (OSNs) in the mammalian nose can detect two distinct modalities transmitted by chemical and mechanical stimuli. As revealed by patch-clamp recordings, many OSNs respond not only to odorants, but also to mechanical stimuli delivered by pressure ejections of odor-free Ringer solution. The mechanical responses correlate directly with the pressure intensity and show several properties similar to those induced by odorants, including onset latency, reversal potential and adaptation to repeated stimulation. Blocking adenylyl cyclase or knocking out the cyclic nucleotide-gated channel CNGA2 eliminates the odorant and the mechanical responses, suggesting that both are mediated by a shared cAMP cascade. We further show that this mechanosensitivity enhances the firing frequency of individual neurons when they are weakly stimulated by odorants and most likely drives the rhythmic activity (theta oscillation) in the olfactory bulb to synchronize with respiration.
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The influence of breathing on brain activity, particularly in the limbic system, appears mostly due to nasal respiration, with the detection of airflow by mechanoreceptors in the olfactory bulb.
“So far, experimental data reveal that the influence of breathing on brain activity, particularly in the limbic system, appears mostly due to nasal respiration 118-120 , with the detection of airflow by mechanoreceptors in the olfactory bulb 121 .”
From Interoceptive rhythms in the brain (2023) · cites this paper as [121]
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Mechanosensory-Based Phase Coding of Odor Identity in the Olfactory Bulb
Iwata, R., Kiyonari, H., & Imai, T. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.008 · Cited by 90 · see citing works
Construction of functional neuronal circuitry in the olfactory bulb
Imai, T. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.07.012 · Cited by 85 · see citing works
Large-scale investigation of the olfactory receptor space using a microfluidic microwell array
Figueroa, X. A., Cooksey, G. A., Votaw, S. V., Horowitz, L. F., & Folch, A. (2010) · Lab on a Chip · doi:10.1039/b920585c · Cited by 86 · see citing works
“2) There is odorant-independent activation, for example a mechanosensitive-OSN response to changes in flow [45] (unlikely as the cells didn’t respond to a pulse of DMSO).”
BackgroundNoto, T., Zhou, G., Schuele, S., Templer, J. W., & Zelano, C. (2018) · Chemical Senses · doi:10.1093/chemse/bjy045 · Cited by 83 · see citing works
Phillips, M. E., Sachdev, R. N. S., Willhite, D. C., & Shepherd, G. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4278-11.2012 · Cited by 86 · see citing works
“Nasal airflow is hypothesized to activate mechanical receptors of ORNs and modulate patterns of excitatory synaptic inputs to OB glomeruli (Spors and Grinvald, 2002; Grosmaitre et al., 2007; Carey et al., 2009; Oka et al., 2009).”
BackgroundFunctional imaging of cortical feedback projections to the olfactory bulb
Rothermel, M., & Wachowiak, M. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00073 · Cited by 83 · see citing works
“Inhalation alone evokes weak OSN inputs to the OB (Grosmaitre et al., 2007; Carey et al., 2009), which are presumably relayed to the AON and which may, as our recordings suggest, trigger inhalation-coupled AON feedback even in the absence of odorant.”
BackgroundRespiratory regulation & interactions with neuro-cognitive circuitry
Maric, V., Ramanathan, D., & Mishra, J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.001 · Cited by 82 · see citing works
Principles of odor coding in vertebrates and artificial chemosensory systems
Manzini, I., Schild, D., & Natale, C. D. (2021) · Physiological Reviews · doi:10.1152/physrev.00036.2020 · Cited by 84 · see citing works
Postnatal Odorant Exposure Induces Peripheral Olfactory Plasticity at the Cellular Level
Cadiou, H., Aoudé, I., Tazir, B., Molinas, A., Fenech, C., Meunier, N., & Grosmaître, X. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0688-13.2014 · Cited by 81 · see citing works
“Distance and pressure were adjusted to minimize mechanical responses (Grosmaitre et al., 2007).”
MethodGrueneberg ganglion neurons respond to cool ambient temperatures
Mamasuew, K., Breer, H., & Fleischer, J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06465.x · Cited by 77 · see citing works
“recently that they do not only respond to odorants but also to mechanical stimuli (Grosmaitre et al., 2007).”
BackgroundRoura, E., Humphrey, B. D., Tedó, G., & Ipharraguerre, I. R. (2008) · Canadian Journal of Animal Science · doi:10.4141/cjas08014 · Cited by 78 · see citing works
Widespread Inhibition, Antagonism, and Synergy in Mouse Olfactory Sensory Neurons In Vivo
Inagaki, S., Iwata, R., Iwamoto, M., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107814 · Cited by 75 · see citing works
“Also, accumulating evidence shows that many OSNs robustly respond to mechanical stimuli produced by the nasal airflow (Chen et al., 2012; Connelly et al., 2015; Grosmaitre et al., 2007; Iwata et al., 2017).”
BackgroundUnravelling the Olfactory Sense: From the Gene to Odor Perception
Teixeira, C. S. S., Cerqueira, N. M. F. S. A., & Ferreira, A. C. S. (2015) · Chemical Senses · doi:10.1093/chemse/bjv075 · Cited by 72 · see citing works
Astroglial Connexin 43 Hemichannels Modulate Olfactory Bulb Slow Oscillations
Roux, L., Madar, A. D., Lacroix, M. M., Yi, C., Benchenane, K., & Giaume, C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0861-15.2015 · Cited by 69 · see citing works
“…et al., 2009) or in vivo after tracheotomy (Ravel and Pager, 1990; Fontanini et al., 2003), pharmacological blockade of the sensory input (Stakic et al., 2011), or uncoupling from the respiratory cycle (Grosmaitre et al., 2007) suggests that slow rhythmic activity is also intrinsic to OB circuits.”
BackgroundThe neuropeptide tachykinin is essential for pheromone detection in a gustatory neural circuit
Shankar, S., Chua, J. Y., Tan, K. J., Calvert, M., Weng, R., Ng, W. C., Mori, K., & Yew, J. Y. (2015) · eLife · doi:10.7554/elife.06914 · Cited by 65 · see citing works
“Similar dual functioning neurons integrating chemical information with touch have been described in nematodes (Kaplan and Horvitz, 1993), mammalian olfactory receptors (Grosmaitre et al., 2007), and vertebrate nociceptor systems (Besson and Chaouch, 1987; Woolf and Walters, 1991).”
BackgroundAvian magnetite-based magnetoreception: a physiologist's perspective
Cadiou, H., & McNaughton, P. A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0423.focus · Cited by 68 · see citing works
Walz, A., Feinstein, P. G., Khan, M., & Mombaerts, P. (2007) · Development · doi:10.1242/dev.008722 · Cited by 67 · see citing works
“The specific function of the septal organ has not been established; its neurons may also have mechanosensory abilities (Grosmaitre et al., 2007).”
BackgroundBrunert, D., Tsuno, Y., Rothermel, M., Shipley, M. T., & Wachowiak, M. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3667-15.2016 · Cited by 65 · see citing works
“1B,D), presumably reflecting responses to weak activation of OSNs by inhalation alone (Grosmaitre et al., 2007; Carey et al., 2009).”
BackgroundConnelly, T., Savigner, A., & Ma, M. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00910.2012 · Cited by 62 · see citing works
“However, because I7 neurons responded to odor-free Ringer solution puffs under this condition, we had to move the puffing pipette to ϳ70 m away to eliminate the mechanical responses elicited by pressure ejection (Grosmaitre et al. 2007).”
MethodSelf-citationCoppola, D. M. (2012) · Neural Plasticity · doi:10.1155/2012/351752 · Cited by 61 · see citing works
“Is not deprivation in an impoverished environment of less moment than deprivation in an enriched environment? Considering these facts it is interesting that OSNs, in addition to responding to odor ligands, are exquisite mechanoreceptors [90].”
BackgroundBetter smelling through genetics: mammalian odor perception
Keller, A., & Vosshall, L. B. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.09.020 · Cited by 61 · see citing works
“Recent work suggests that the septal organ is both broadly tuned to various volatile odors and also shows a unique sensitivity to mechanical stimulation [38].”
BackgroundLi, A., Gire, D. H., & Restrepo, D. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4003-14.2015 · Cited by 61 · see citing works
“In addition, in the frequency, the LFP partially follows sniffing (Grosmaitre et al., 2007; Rosero and Aylwin, 2011; Gschwend et al., 2012; Khan et al., 2012), and sniffing has been postulated to provide a temporal basis to extract odor identity (Cury and Uchida, 2010; Shusterman et al.”
BackgroundGrueneberg Ganglion Neurons Are Finely Tuned Cold Sensors
Schmid, A., Pyrski, M. M., Biel, M., Leinders‐Zufall, T., & Zufall, F. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0608-10.2010 · Cited by 61 · see citing works
“The most intriguing explanation is that GGNs may act as multimodal sensors that are responsive to both thermo- and chemostimuli, thus joining an only recently discovered group of mammalian olfactory neurons with dual or multiple functions (Grosmaitre et al., 2007; Zufall and Munger, 2010).”
BackgroundPietra, G., Dibattista, M., Menini, A., Reisert, J., & Boccaccio, A. (2016) · The Journal of General Physiology · doi:10.1085/jgp.201611622 · Cited by 61 · see citing works
Olfactory bulb coding of odors, mixtures and sniffs is a linear sum of odor time profiles
Gupta, P., Albeanu, D. F., & Bhalla, U. S. (2015) · Nature Neuroscience · doi:10.1038/nn.3913 · Cited by 60 · see citing works
Expression patterns of anoctamin 1 and anoctamin 2 chloride channels in the mammalian nose
Dauner, K., Lißmann, J., Jeridi, S., Frings, S., & Möhrlen, F. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1324-9 · Cited by 59 · see citing works
“On the basis of its broad spectrum for odor detection (Marshall and Maruniak 1986 ), the pronounced mechanosensitivity of its ORNs (Grosmaitre et al. 2007) and its distinct projection pattern to the ventral olfactory bulb (Levai and Strotmann 2003), the SO has been suggested to raise alertness to…”
BackgroundOka, Y., Takai, Y., & Touhara, K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1415-09.2009 · Cited by 58 · see citing works
“Recent in vitro electrophysiological study has shown that OSNs have the ability to respond to mechanical stimulation, suggesting that mechanical and odorant responses may be integrated in the OSN (Grosmaitre et al., 2007).”
BackgroundChen, M., Chen, Y., Huo, Q., Wang, L., Tan, S., Misrani, A., Jiang, J., Chen, J., Chen, S., Zhang, J., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00434-7 · Cited by 61 · see citing works
“Thus, a reduction in the number of mature OSNs would result in less glutamatergic innervation of M/T cells, leading to reduced excitation and theta oscillations seen in the present study [52, 53], in addition to decreased EOG amplitude.”
BackgroundOlfactory modulation of the medial prefrontal cortex circuitry: Implications for social cognition
Bhattarai, J. P., Etyemez, S., Jaaro-Peled, H., Janke, E., Tolosa, U. D. L., Kamiya, A., Gottfried, J. A., Sawa, A., & Ma, M. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.03.022 · Cited by 56 · see citing works
Self-citationWang, J., & Hamill, O. P. (2021) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2004085 · Cited by 55 · see citing works
Genetics of canine olfaction and receptor diversity
Quignon, P., Rimbault, M., Robin, S., & Galibert, F. (2011) · Mammalian Genome · doi:10.1007/s00335-011-9371-1 · Cited by 57 · see citing works
“For example, Masera’s organ, which expresses only a fraction of the OR repertoire (Kaluza et al. 2004; Tian and Ma 2004), is extremely sensitive to a wide variety of odorant stimuli (Grosmaitre et al. 2007; Marshall and Maruniak 1986).”
BackgroundThe deep and slow breathing characterizing rest favors brain respiratory-drive
Girin, B., Juventin, M., Garcia, S., Lefèvre, L., Amat, C., Fourcaud‐Trocmé, N., & Buonviso, N. (2021) · Scientific Reports · doi:10.1038/s41598-021-86525-3 · Cited by 57 · see citing works
How to monitor breathing in laboratory rodents: a review of the current methods
Grimaud, J., & Murthy, V. N. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00708.2017 · Cited by 56 · see citing works
“These observations make sense, since OB -cycles result from air movements on the olfactory epithelium, at the back of the nasal cavity (Grosmaitre et al. 2007).”
BackgroundMultimodal sensory processing in Caenorhabditis elegans
Metaxakis, A., Petratou, D., & Tavernarakis, N. (2018) · Open Biology · doi:10.1098/rsob.180049 · Cited by 58 · see citing works
Precise Synaptic Balance in the Zebrafish Homolog of Olfactory Cortex
Rupprecht, P., & Friedrich, R. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.013 · Cited by 57 · see citing works
Compensatory Rapid Switching of Binasal Inputs in the Olfactory Cortex
Kikuta, S., Kashiwadani, H., & Mori, K. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3106-08.2008 · Cited by 56 · see citing works
“In the absence of odor stimulation, 27% (119 of 440 cells recorded) of AON neurons showed respiration phase-locked spike discharges which were presumably induced by room air odorants or periodic mechanical stimulation of the olfactory sensory neurons resulting from nasal airflow (Grosmaitre et al., 2007).”
BackgroundRespiration-Driven Brain Oscillations in Emotional Cognition
Folschweiller, S., & Sauer, J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.761812 · Cited by 54 · see citing works
Activity-Dependent Modulation of Odorant Receptor Gene Expression in the Mouse Olfactory Epithelium
Zhao, S., Tian, H., Ma, L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069862 · Cited by 53 · see citing works
“A subset of OSNs in the mouse olfactory epithelium can respond to mechanical stimulation in addition to odors [45].”
BackgroundSelf-citationKarunanayaka, P., Eslinger, P. J., Wang, J., Weitekamp, C. W., Molitoris, S., Gates, K. M., Molenaar, P. C. M., & Yang, Q. X. (2013) · Human Brain Mapping · doi:10.1002/hbm.22312 · Cited by 52 · see citing works
“These data are consistent with other no-odor or “sniff-related” activity that has been observed at (1) the olfactory epithelium [Grosmaitre et al., 2007]; (2) the bulb [Adrian, 1942]; and (3) the cortex [Sobel et al., 1998a,b; Zelano and Sobel, 2005].”
Temporal Relations between Cortical Network Oscillations and Breathing Frequency during REM Sleep
Tort, A. B. L., Hammer, M., Zhang, J., Brankačk, J., & Draguhn, A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3067-20.2021 · Cited by 48 · see citing works
“It is worth noticing that this drive is also provided by the mechanical stimulation through nasal air movement, even in the absence of odors (Grosmaitre et al., 2007; Connelly et al., 2015).”
BackgroundGrueneberg Ganglion Neurons Are Activated by a Defined Set of Odorants
Mamasuew, K., Hofmann, N., Breer, H., & Fleischer, J. (2010) · Chemical Senses · doi:10.1093/chemse/bjq124 · Cited by 50 · see citing works
“For these cells, it has been proposed that an increased airflow in the nose during sniffing could mechanically sensitize these neurons for a chemical stimulus (Grosmaitre et al. 2007).”
BackgroundBravin, C., Guidetti, A., Licini, G., et al. (2019) · Chemical Science · doi:10.1039/c8sc05527k · Cited by 50 · see citing works
Odor Representations in the Rat Olfactory Bulb Change Smoothly with Morphing Stimuli
Khan, A. G., Thattai, M., & Bhalla, U. S. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.008 · Cited by 50 · see citing works
“Patterned activity to air alone may be explained by recent work on mechanosensitive properties of ORNs (Grosmaitre et al., 2007).”
Rojas-Líbano, D., Wimmer del Solar, J., Aguilar-Rivera, M., Montefusco-Siegmund, R., & Maldonado, P. E. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00088.2018 · Cited by 46 · see citing works
“In this case, the mechanical impact of the air in the nose upon each breath cycle is picked up by the olfactory sensory neurons (Grosmaitre et al. 2007), which results in the neural OB’s respiratory rhythm.”
BackgroundOlfactory Stimulation Regulates the Birth of Neurons That Express Specific Odorant Receptors
van der Linden, C. J., Gupta, P., Bhuiya, A. I., Riddick, K. R., Hossain, K., & Santoro, S. W. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108210 · Cited by 49 · see citing works
“To do so, we used UNO, a procedure that provides a simple method for reproducibly reducing olfactory stimulation (broadly defined here as both odor- and mechanically derived; Grosmaitre et al., 2007) on the closed side of the OE, as well as a within-animal control (the open side of the OE).”
BackgroundMethodPiarulli, A., Zaccaro, A., Laurino, M., Menicucci, D., De Vito, A., Bruschini, L., Berrettini, S., Bergamasco, M., Laureys, S., & Gemignani, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-24924-9 · Cited by 52 · see citing works
“As anticipated in the Introduction, the aim of the study was that of driving brain electrical activity and modulating consciousness by delivering rhythmic pressurized-air stimulations to the olfactory epithelium, whose receptors have been shown to be sensitive also to mechanical stimuli 4 .”
Cranial Pair I: The Olfactory Nerve
Crespo, C., Liberia, T., Blasco‐Ibáñez, J. M., Nácher, J., & Varea, E. (2018) · The Anatomical Record · doi:10.1002/ar.23816 · Cited by 48 · see citing works
Yang, Q., Zhou, G., Noto, T., Templer, J. W., Schuele, S., Rosenow, J. M., Lane, G., & Zelano, C. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001509 · Cited by 47 · see citing works
Functional somatic syndromes, anxiety disorders and the upper airway: A matter of paradigms
Gold, A. R. (2011) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2010.11.004 · Cited by 45 · see citing works
Huang, J. S., Kunkhyen, T., Rangel, A. N., Brechbill, T. R., Gregory, J. D., Winson-Bushby, E. D., Liu, B., Avon, J. T., Muggleton, R. J., & Cheetham, C. E. J. (2022) · Nature Communications · doi:10.1038/s41467-022-33967-6 · Cited by 46 · see citing works
Global coordination of brain activity by the breathing cycle
Tort, A. B. L., Laplagne, D. A., Draguhn, A., & González, J. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00920-7 · Cited by 55 · see citing works
“Indeed, these neurons respond not only to odorant binding but also to mechanical (pressure) stimuli 182 , with both mechanosensitivity and chemosensitivity being mediated by the same membrane receptors 182,183 .”
Signaling by olfactory receptor neurons near threshold
Bhandawat, V., Reisert, J., & Yau, K. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004571107 · Cited by 46 · see citing works
- Authors
- Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M., & Ma, M.
- Affiliations
- Istituto Nazionale di Geofisica e Vulcanologia (IT)
- World Bank (US)
- Jet Propulsion Laboratory (US)
- University of Pennsylvania (US)
- Corresponding author
- Ma, Minghong
- Venue
- Nature Neuroscience
- Published
- 2007-02-18
- Volume
- 10
- Issue
- 3
- Pages
- 348-354
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC2227320
- OpenAlex
- W2120729067
- Semantic Scholar
- 54917ce60e3e9e3ade1f6a0be8605b162006b36d
- Cited by
- 371
- References
- 38
- Citations by year
- 2026: 16 · 2025: 26 · 2024: 27 · 2023: 23 · 2022: 23 · 2021: 39 · 2020: 20 · 2019: 16 · 2018: 29 · 2017: 11 · 2016: 18 · 2015: 14 · 2014: 20 · 2013: 18 · 2012: 11
- FWCI
- 7.18
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Funders
- Whitehall Foundation
- University of Pennsylvania
- Johns Hopkins University
- National Institute on Deafness and Other Communication Disorders (R01DC006213)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- olfactory sensory neurons, mechanosensitivity, odor detection, cyclic nucleotide-gated channels, CNGA2, adenylate cyclase, cAMP signaling, neural adaptation, theta oscillations, olfactory bulb, neuronal firing rate
- MeSH terms
- Cyclic AMP, Animals, Dose-Response Relationship, Radiation, Enzyme Inhibitors, Female, Imines, Ion Channels, Male, Membrane Potentials, Neurons, Afferent, Odorants, Olfactory Bulb, Physical Stimulation, Smell, Stimulation, Chemical, Touch, Mice, Knockout, Patch-Clamp Techniques, Mice, Cyclic Nucleotide-Gated Cation Channels, In Vitro Techniques
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