An olfactory cocktail party: figure-ground segregation of odorants in rodents

In odorant-rich environments, animals must be able to detect specific odorants of interest against variable backgrounds. However, studies have found that both humans and rodents are poor at analyzing the components of odorant mixtures, suggesting that olfaction is a synthetic sense in which mixtures are perceived holistically. We found that mice could be easily trained to detect target odorants embedded in unpredictable and variable mixtures. To relate the behavioral performance to neural representation, we imaged the responses of olfactory bulb glomeruli to individual odors in mice expressing the Ca2+ indicator GCaMP3 in olfactory receptor neurons. The difficulty of segregating the target from the background depended strongly on the extent of overlap between the glomerular responses to target and background odors. Our study indicates that the olfactory system has powerful analytic abilities that are constrained by the limits of combinatorial neural representation of odorants at the level of the olfactory receptors.

[1]  W. Howard,et al.  Food detection by deer mice using olfactory rather than visual cues. , 1968, Animal behaviour.

[2]  E. Polak Mutiple profile-multiple receptor site model for vertebrate olfaction. , 1973, Journal of theoretical biology.

[3]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[4]  A. Blaustein Sexual Selection and Mammalian Olfaction , 1981, The American Naturalist.

[5]  D. G. Laing,et al.  The capacity of humans to identify odors in mixtures , 1989, Physiology & Behavior.

[6]  M. Laska,et al.  Determinants of Odor Mixture Perception in Squirrel Monkeys, Saimiri sciureus , 1994 .

[7]  M. Landy,et al.  Examining edge- and region-based texture analysis mechanisms , 1998, Vision Research.

[8]  D. G. Laing,et al.  A Limit in the Processing of Components in Odour Mixtures , 1999, Perception.

[9]  J J Hopfield,et al.  Odor space and olfactory processing: collective algorithms and neural implementation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[11]  D. G. Laing,et al.  The analysis of odor mixtures by humans: evidence for a configurational process , 2001, Physiology & Behavior.

[12]  T. Bonhoeffer,et al.  Tuning and Topography in an Odor Map on the Rat Olfactory Bulb , 2001, The Journal of Neuroscience.

[13]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.

[14]  Frédéric Berthommier,et al.  Mitral cell temporal response patterns evoked by odor mixtures in the rat olfactory bulb. , 2002, Journal of neurophysiology.

[15]  C. Linster,et al.  Configurational and nonconfigurational interactions between odorants in binary mixtures. , 2003, Behavioral neuroscience.

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

[17]  Carlos D. Brody,et al.  Simple Networks for Spike-Timing-Based Computation, with Application to Olfactory Processing , 2003, Neuron.

[18]  Donald A. Wilson,et al.  Olfactory perceptual learning: the critical role of memory in odor discrimination , 2003, Neuroscience & Biobehavioral Reviews.

[19]  M. Laska,et al.  Discriminating parts from the whole: determinants of odor mixture perception in squirrel monkeys, Saimiri sciureus , 1993, Journal of Comparative Physiology A.

[20]  Rainer W Friedrich,et al.  Processing of Odor Mixtures in the Zebrafish Olfactory Bulb , 2004, The Journal of Neuroscience.

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

[22]  Leslie M Kay,et al.  A redefinition of odor mixture quality. , 2005, Behavioral neuroscience.

[23]  R. Apfelbach,et al.  The effects of predator odors in mammalian prey species: A review of field and laboratory studies , 2005, Neuroscience & Biobehavioral Reviews.

[24]  Matt Wachowiak,et al.  Odorant Representations Are Modulated by Intra- but Not Interglomerular Presynaptic Inhibition of Olfactory Sensory Neurons , 2005, Neuron.

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

[26]  Lawrence C. Katz,et al.  Representation of Natural Stimuli in the Rodent Main Olfactory Bulb , 2006, Neuron.

[27]  Donald A. Wilson,et al.  Synaptic adaptation and odor-background segmentation , 2007, Neurobiology of Learning and Memory.

[28]  A. Gelperin,et al.  Olfactory coding with all-or-nothing glomeruli. , 2007, Journal of neurophysiology.

[29]  N. Issa,et al.  Glomerular activation patterns and the perception of odor mixtures , 2008, The European journal of neuroscience.

[30]  Michael Davis,et al.  Learning-Dependent Structural Plasticity in the Adult Olfactory Pathway , 2008, The Journal of Neuroscience.

[31]  Mounya Elhilali,et al.  A cocktail party with a cortical twist: how cortical mechanisms contribute to sound segregation. , 2008, The Journal of the Acoustical Society of America.

[32]  Donald A Wilson,et al.  Olfactory perceptual stability and discrimination , 2008, Nature Neuroscience.

[33]  Donald A. Wilson,et al.  Pattern Separation and Completion in Olfaction , 2009, Annals of the New York Academy of Sciences.

[34]  Josh H. McDermott The cocktail party problem , 2009, Current Biology.

[35]  Leslie M Kay,et al.  A critical test of the overlap hypothesis for odor mixture perception. , 2009, Behavioral neuroscience.

[36]  Markus Meister,et al.  Precision and diversity in an odor map on the olfactory bulb , 2009, Nature Neuroscience.

[37]  Thomas Serre,et al.  What are the Visual Features Underlying Rapid Object Recognition? , 2011, Front. Psychology.

[38]  Dmitry Rinberg,et al.  In search of the structure of human olfactory space. , 2011, Frontiers in systems neuroscience.

[39]  M. Fletcher,et al.  Analytical Processing of Binary Mixture Information by Olfactory Bulb Glomeruli , 2011, PloS one.

[40]  V. Murthy,et al.  Molecular Organization of Vomeronasal Chemoreception , 2011, Nature.

[41]  Dan D. Stettler,et al.  Driving Opposing Behaviors with Ensembles of Piriform Neurons , 2011, Cell.

[42]  V. Murthy,et al.  Functional Properties of Cortical Feedback Projections to the Olfactory Bulb , 2012, Neuron.

[43]  Donald A. Wilson,et al.  Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity , 2011, Nature Neuroscience.

[44]  Winfried Wiegraebe,et al.  Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb , 2012, Proceedings of the National Academy of Sciences.

[45]  Jeffry S. Isaacson,et al.  Cortical Feedback Control of Olfactory Bulb Circuits , 2012, Neuron.

[46]  T. Holy,et al.  Robust Encoding of Stimulus Identity and Concentration in the Accessory Olfactory System , 2013, The Journal of Neuroscience.

[47]  G. Laurent,et al.  Encoding of Mixtures in a Simple Olfactory System , 2013, Neuron.

[48]  Naoshige Uchida,et al.  The Limits of Deliberation in a Perceptual Decision Task , 2013, Neuron.

[49]  Steven M. Peterson,et al.  A spatiotemporal coding mechanism for background-invariant odor recognition , 2013, Nature Neuroscience.

[50]  J. McGann,et al.  Odor-Specific, Olfactory Marker Protein-Mediated Sparsening of Primary Olfactory Input to the Brain after Odor Exposure , 2013, The Journal of Neuroscience.

[51]  N. Sobel,et al.  The perceptual logic of smell , 2014, Current Opinion in Neurobiology.

[52]  Alan Carleton,et al.  Long term functional plasticity of sensory inputs mediated by olfactory learning , 2014, eLife.

[53]  D. S. M A X W E L L,et al.  B Y H E a V Y I O N I Z I N G P a R T I C L E S , 2022 .