Olfactory receptor neuron responses coding for rapid odour sampling

Non‐technical summary  Odorants are transported into the nasal cavity upon air inhalation where they are detected by olfactory receptor neurons (ORNs), which transduce the odorant molecules into action potentials. The rate of stimulation thus depends on the chosen breathing frequency, which in mice ranges from 2 to 10 Hz. This poses the question how ORNs respond to rapidly changing stimulation rates. Individual mouse ORNs respond reliably to repetitive 2 Hz stimulations resembling normal breathing, but actually perform much poorer when the stimulation rate is increased to 5 Hz, which is more akin to sniffing. In this case, rarely more than 50% of the stimulations elicit any response, with an increase in odorant concentration further reducing the response rate, becoming zero at high concentrations. This counterintuitive observation can be understood in the framework of an adaptive filter, which allows the animal to selectively alter its ORN output depending on the chosen breathing rate.

[1]  U. Kaupp Olfactory signalling in vertebrates and insects: differences and commonalities , 2010, Nature Reviews Neuroscience.

[2]  Haiqing Zhao,et al.  Phosphodiesterase 1C is dispensable for rapid response termination of olfactory sensory neurons , 2009, Nature Neuroscience.

[3]  Serge Charpak,et al.  Peripheral Adaptation Codes for High Odor Concentration in Glomeruli , 2009, The Journal of Neuroscience.

[4]  Ryan M Carey,et al.  Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. , 2009, Journal of neurophysiology.

[5]  S. J. Kleene,et al.  The electrochemical basis of odor transduction in vertebrate olfactory cilia. , 2008, Chemical senses.

[6]  J. Reisert,et al.  Olfactory CNG Channel Desensitization by Ca2+/CaM via the B1b Subunit Affects Response Termination but Not Sensitivity to Recurring Stimulation , 2008, Neuron.

[7]  Ryan M Carey,et al.  Rapid Encoding and Perception of Novel Odors in the Rat , 2008, PLoS biology.

[8]  J. Rospars,et al.  Competitive and Noncompetitive Odorant Interactions in the Early Neural Coding of Odorant Mixtures , 2008, The Journal of Neuroscience.

[9]  Alan Carleton,et al.  Dynamic Ensemble Odor Coding in the Mammalian Olfactory Bulb: Sensory Information at Different Timescales , 2008, Neuron.

[10]  K. Yau,et al.  Olfactory marker protein modulates the cAMP kinetics of the odour‐induced response in cilia of mouse olfactory receptor neurons , 2007, The Journal of physiology.

[11]  Adam Kepecs,et al.  Rapid and precise control of sniffing during olfactory discrimination in rats. , 2007, Journal of neurophysiology.

[12]  H. R. Matthews,et al.  The effect of external sodium concentration on sodium–calcium exchange in frog olfactory receptor cells , 2007, The Journal of physiology.

[13]  J. White,et al.  Sniffing controls an adaptive filter of sensory input to the olfactory bulb , 2007, Nature Neuroscience.

[14]  Troy W. Margrie,et al.  Spatiotemporal representations in the olfactory system , 2007, Trends in Neurosciences.

[15]  J. Caprio,et al.  Responses of olfactory forebrain units to amino acids in the channel catfish. , 2007, Journal of neurophysiology.

[16]  Y. Yoshihara,et al.  Odorant Receptor Map in the Mouse Olfactory Bulb: In Vivo Sensitivity and Specificity of Receptor-Defined Glomeruli , 2006, Neuron.

[17]  Alan Gelperin,et al.  Sparse Odor Coding in Awake Behaving Mice , 2006, The Journal of Neuroscience.

[18]  A. Gelperin,et al.  Speed-Accuracy Tradeoff in Olfaction , 2006, Neuron.

[19]  A. Menini,et al.  Fast Adaptation in Mouse Olfactory Sensory Neurons Does Not Require the Activity of Phosphodiesterase , 2006, The Journal of general physiology.

[20]  Adam Kepecs,et al.  The sniff as a unit of olfactory processing. , 2006, Chemical senses.

[21]  Noam Sobel,et al.  The sniff is part of the olfactory percept. , 2006, Chemical senses.

[22]  Thomas A. Cleland,et al.  The anatomical logic of smell , 2005, Trends in Neurosciences.

[23]  K. Yau,et al.  Elementary Response of Olfactory Receptor Neurons to Odorants , 2005, Science.

[24]  Andreas T. Schaefer,et al.  Maintaining Accuracy at the Expense of Speed Stimulus Similarity Defines Odor Discrimination Time in Mice , 2004, Neuron.

[25]  Z. Mainen,et al.  Speed and accuracy of olfactory discrimination in the rat , 2003, Nature Neuroscience.

[26]  J. Rospars,et al.  Relation between stimulus and response in frog olfactory receptor neurons in vivo , 2003, The European journal of neuroscience.

[27]  Jianhua Cang,et al.  In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb , 2003, The Journal of Neuroscience.

[28]  Peter Mombaerts,et al.  Odorant Receptor Expression Defines Functional Units in the Mouse Olfactory System , 2002, The Journal of Neuroscience.

[29]  J. Reisert,et al.  Responses to prolonged odour stimulation in frog olfactory receptor cells , 2001, The Journal of physiology.

[30]  J. Reisert,et al.  Response properties of isolated mouse olfactory receptor cells , 2001, The Journal of physiology.

[31]  Gilles Laurent,et al.  Odor- and context-dependent modulation of mitral cell activity in behaving rats , 1999, Nature Neuroscience.

[32]  Gordon M Shepherd,et al.  Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation , 1999, Journal of Neuroscience Methods.

[33]  J. Reisert,et al.  Adaptation of the odour‐induced response in frog olfactory receptor cells , 1999, The Journal of physiology.

[34]  J. Reisert,et al.  Na+-dependent Ca2+ Extrusion Governs Response Recovery in Frog Olfactory Receptor Cells , 1998, The Journal of general physiology.

[35]  S. Frings,et al.  A Depolarizing Chloride Current Contributes to Chemoelectrical Transduction in Olfactory Sensory Neurons In Situ , 1998, The Journal of Neuroscience.

[36]  J. D. E. Gabrieli,et al.  Sniffing and smelling: separate subsystems in the human olfactory cortex , 1998, Nature.

[37]  F. Kawai,et al.  Quantitative analysis of Na+ and Ca2+ current contributions on spike initiation in the newt olfactory receptor cell. , 1997, The Japanese journal of physiology.

[38]  James M. Bower,et al.  Multiday Recordings from Olfactory Bulb Neurons in Awake Freely Moving Rats: Spatially and Temporally Organized Variability in Odorant Response Properties , 1997, Journal of Computational Neuroscience.

[39]  S. Kleeberger,et al.  Differential control of ventilation among inbred strains of mice. , 1994, The American journal of physiology.

[40]  D. Trotier,et al.  Intensity coding in olfactory receptor cells. , 1994, Seminars in cell biology.

[41]  D. Tank,et al.  Timing of odor stimulation does not alter patterning of olfactory bulb unit activity in freely breathing rats. , 1993, Journal of neurophysiology.

[42]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

[43]  F. Berthommier,et al.  Temporal Patterns in Spontaneous and Odour‐evoked Mitral Cell Discharges Recorded in Anaesthetized Freely Breathing Animals , 1992, The European journal of neuroscience.

[44]  G. Lowe,et al.  The spatial distributions of odorant sensitivity and odorant‐induced currents in salamander olfactory receptor cells. , 1991, The Journal of physiology.

[45]  David E. Hornung,et al.  A quantitative analysis of sniffing strategies in rats performing odor detection tasks , 1987, Physiology & Behavior.

[46]  A. Holley,et al.  Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits , 1985, Physiology & Behavior.

[47]  A. Holley,et al.  Receptor cell responses to odorants: Similarities and differences among odorants , 1984, Brain Research.

[48]  D. G. Laing,et al.  Natural Sniffing Gives Optimum Odour Perception for Humans , 1983, Perception.

[49]  G. Shepherd,et al.  Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. , 1978, The Journal of physiology.

[50]  W. Drongelen,et al.  Unitary recordings of near threshold responses of receptor cells in the olfactory mucosa of the frog. , 1978, The Journal of physiology.

[51]  Stephan L. Chorover,et al.  Response plasticity in hamster olfactory bulb: peripheral and central processes , 1976, Brain Research.

[52]  F. Macrides,et al.  Olfactory Bulb Units: Activity Correlated with Inhalation Cycles and Odor Quality , 1972, Science.

[53]  J Y Lettvin,et al.  Chemical transmission in the nose of the frog. , 1965, The Journal of physiology.

[54]  T. Shibuya,et al.  Olfactory Epithelium: Unitary Responses in the Tortoise , 1963, Science.

[55]  J. Caprio,et al.  Odorant specificity of single olfactory bulb neurons to amino acids in the channel catfish. , 2004, Journal of neurophysiology.

[56]  J. Champagnat,et al.  Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. , 1995, Physiological reviews.

[57]  K. Imamura,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. , 1992, Journal of neurophysiology.

[58]  J. DU PONT,et al.  Firing patterns of bulbar respiratory neurones during sniffing in the conscious, non-paralyzed rabbit. , 1987, Brain research.