Abstract
Animals rarely encounter odors in isolation, and their olfactory systems generally operate in the context of complex mixtures of odorants. Individual objects typically emit a multitude of volatile chemicals that become their signature for identification. In addition, chemicals emitted from multiple objects mix in the air before reaching the nose. There is great interest, therefore, in understanding how mixtures are processed by the olfactory system to allow perceiving objects and segregating them from background odors. Studies comparing the neural responses to single odorants and their mixtures show that it is often not easy to predict the mixture response from the components, suggesting that cross-odorant interactions take place at multiple levels of the mammalian olfactory system. Experiments that relate cross-odorant interactions to perception may elucidate how mixture processing underlies object identification and background segregation.
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References
Abaffy T, Matsunami H, Luetje CW (2006) Functional analysis of a mammalian odorant receptor subfamily. J Neurochem 97:1506–1518
Araneda RC, Kini AD, Firestein S (2000) The molecular receptive range of an odorant receptor. Nat Neurosci 3:1248–1255
Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre–surround inhibition among olfactory bulb glomeruli. Nature 426:623–629
Axel R (1995) The molecular logic of smell. Sci Am 273:154–159
Banerjee A, Marbach F, Anselmi F, Koh MS, Davis MB, Garcia da Silva P, Delevich K, Oyibo HK, Gupta P, Li B et al (2015) An interglomerular circuit gates glomerular output and implements gain control in the mouse olfactory bulb. Neuron 87:193–207
Barnes DC, Hofacer RD, Zaman AR, Rennaker RL, Wilson DA (2008) Olfactory perceptual stability and discrimination. Nat Neurosci 11:1378–1380
Belluscio L, Katz LC (2001) Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21:2113–2122
Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174
Cain WS (1975) Odor intensity: mixtures and masking. Chem Senses Flavor 1:339–352
Chapuis J, Wilson DA (2012) Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15:155–161
Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R (2011) Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1004–1015
Cleland TA (2014) Construction of odor representations by olfactory bulb microcircuits. Prog Brain Res 208:177–203. https://doi.org/10.1016/B978-0-444-63350-7.00007-3
Coureaud G, Thomas-Danguin T, Le Berre E, Schaal B (2008) Perception of odor blending mixtures in the newborn rabbit. Physiol Behav 95:194–199
Davison IG, Katz LC (2007) Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J Neurosci 27:2091–2101
Deisig N, Giurfa M, Sandoz JC (2010) Antennal lobe processing increases separability of odor mixture representations in the Honeybee. J Neurophysiol 103:2185–2194
Doucette W, Restrepo D (2008) Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol 6:e258
Duchamp-Viret P, Duchamp A, Chaput MA (2003) Single olfactory sensory neurons simultaneously integrate the components of an odour mixture. Eur J Neurosci 18:2690–2696
Effmert U, Große J, Röse USR, Ehrig F, Kägi R, Piechulla B (2005) Volatile composition, emission pattern, and localization of floral scent emission in Mirabilis jalapa (Nyctaginaceae). Am J Bot 92:2–12
Fantana AL, Soucy ER, Meister M (2008) Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59:802–814
Fletcher ML (2011) Analytical processing of binary mixture information by olfactory bulb glomeruli. PLoS One 6:e29360
Franks KM, Russo MJ, Sosulski DL, Mulligan AA, Siegelbaum SA, Axel R (2011) Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72:49–56
Fu X, Yan Y, Xu PS, Geerlof-Vidavsky I, Chong W, Gross ML, Holy TE (2015) A molecular code for identity in the vomeronasal system. Cell 163:313–323
Giessel AJ, Datta SR (2014) Olfactory maps, circuits and computations. Curr Opin Neurobiol 24:120–132
Giraudet P, Berthommier F, Chaput M (2002) Mitral cell temporal response patterns evoked by odor mixtures in the rat olfactory bulb. J Neurophysiol 88:829–838
Grosmaitre X, Fuss SH, Lee AC, Adipietro KA, Matsunami H, Mombaerts P, Ma M (2009) SR1, a mouse odorant receptor with an unusually broad response profile. J Neurosci 29:14545–14552
Grossman KJ, Mallik AK, Ross J, Kay LM, Issa NP (2008) Glomerular activation patterns and the perception of odor mixtures. Eur J Neurosci 27:2676–2685
Gupta P, Albeanu DF, Bhalla US (2015) Olfactory bulb coding of odors, mixtures and sniffs is a linear sum of odor time profiles. Nat Neurosci 18:272–281
Jinks A, Laing DG (1999) A limit in the processing of components in odour mixtures. Perception 28:395–404
Jinks A, Laing DG (2001) The analysis of odor mixtures by humans: evidence for a configurational process. Physiol Behav 72:51–63
Johnson DMG, Illig KR, Behan M, Haberly LB (2000) New features of connectivity in piriform cortex visualized by intracellular injection of Pyramidal Cells Suggest that “Primary” olfactory cortex functions like “Association” cortex in other sensory systems. J Neurosci 20:6974–6982
Jones FN, Woskow MH (1964) On the intensity of odor mixtures. Ann N Y Acad Sci 116:484–494
Kadohisa M, Wilson DA (2006) Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 95:1888–1896
Kaeppler K, Mueller F (2013) Odor classification: a review of factors influencing perception-based odor arrangements. Chem Senses 38:189–209
Kajiya K, Inaki K, Tanaka M, Haga T, Kataoka H, Touhara K (2001) Molecular bases of odor discrimination: reconstitution of olfactory receptors that recognize overlapping sets of odorants. J Neurosci 21:6018–6025
Kato HK, Chu MW, Isaacson JS, Komiyama T (2012) Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76:962–975
Kay LM, Lowry CA, Jacobs HA (2003) Receptor contributions to configural and elemental odor mixture perception. Behav Neurosci 117:1108–1114
Kay LM, Crk T, Thorngate J (2005) A redefinition of odor mixture quality. Behav Neurosci 119:726–733
Khan RM, Luk C-H, Flinker A, Aggarwal A, Lapid H, Haddad R, Sobel N (2007) Predicting odor pleasantness from odorant structure: pleasantness as a reflection of the physical world. J Neurosci 27:10015–10023
Koulakov AA, Enikolopov AG and Rinberg D (2009) The structure of human olfactory space. ArXiv: 0907.3964 Q-Bio
Kurahashi T, Lowe G, Gold GH (1994) Suppression of odorant responses by odorants in olfactory receptor cells. Science 265:118–120
Laing DG, Francis GW (1989) The capacity of humans to identify odors in mixtures. Physiol Behav 46:809–814
Laing DG, Glemarec A (1992) Selective attention and the perceptual analysis of odor mixtures. Physiol Behav 52:1047–1053
Laing DG, Panhuber H, Willcox ME, Pittman EA (1984) Quality and intensity of binary odor mixtures. Physiol Behav 33:309–319
Lawless HT (1999) Descriptive analysis of complex odors: reality, model or illusion? Food Qual Prefer 10:325–332
Lei H, Mooney R, Katz LC (2006) Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J Neurosci Off J Soc Neurosci 26:12023–12032
Li W, Luxenberg E, Parrish T, Gottfried JA (2006) Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52:1097–1108
Lin DY, Shea SD, Katz LC (2006) Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50:937–949
Linster C, Cleland TA (2004) Configurational and elemental odor mixture perception can arise from local inhibition. J Comput Neurosci 16:39–47
Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723
Marasco A, De Paris A, Migliore M (2016) Predicting the response of olfactory sensory neurons to odor mixtures from single odor response. Sci, Rep, p 6
Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76:1175–1188
Mathis A, Rokni D, Kapoor V, Bethge M, Murthy VN (2016) Reading out olfactory receptors: feed forward circuits detect odors in mixtures without demixing. Neuron 91:1110–1123
Mayer F, Grosch W (2001) Aroma simulation on the basis of the odourant composition of roasted coffee headspace. Flavour Fragr J. 16:180–190
McGann JP, Pírez N, Gainey MA, Muratore C, Elias AS, Wachowiak M (2005) Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48:1039–1053
Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR, Taniguchi H, Tasic B, Huang ZJ, He Z et al (2011) Cortical representations of olfactory input by trans-synaptic tracing. Nature 472:191–196
Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278
Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686
Monahan K, Lomvardas S (2015) Monoallelic expression of olfactory receptors. Annu Rev Cell Dev Biol 31:721–740
Namiki S, Iwabuchi S, Kanzaki R (2008) Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori. J Comp Physiol A 194:501–515
Oka Y, Omura M, Kataoka H, Touhara K (2004) Olfactory receptor antagonism between odorants. EMBO J 23:120–126
Olender T, Lancet D, Nebert DW (2008) Update on the olfactory receptor (OR) gene superfamily. Hum Genom 3:87–97
Otazu GH, Chae H, Davis MB, Albeanu DF (2015) Cortical feedback decorrelates olfactory bulb output in awake mice. Neuron 86:1461–1477
Poo C, Isaacson JS (2009) Odor representations in olfactory cortex: “Sparse” coding, global inhibition, and oscillations. Neuron 62:850–861
Rokni D, Hemmelder V, Kapoor V, Murthy VN (2014) An olfactory cocktail party: figure-ground segregation of odorants in rodents. Nat Neurosci 17:1225–1232
Rospars J-P, Lansky P, Chaput M, Duchamp-Viret P (2008) Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures. J Neurosci 28:2659–2666
Saha D, Leong K, Li C, Peterson S, Siegel G, Raman B (2013) A spatiotemporal coding mechanism for background-invariant odor recognition. Nat Neurosci 16:1830–1839
Shahidi F, Rubin LJ, D’Souza LA, Teranishi R, Buttery RG (1986) Meat flavor volatiles: a review of the composition, techniques of analysis, and sensory evaluation. CRC Crit Rev Food Sci Nutr 24:141–243
Shen K, Tootoonian S, Laurent G (2013) Encoding of mixtures in a simple olfactory system. Neuron 80:1246–1262
Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977
Stettler DD, Axel R (2009) Representations of odor in the piriform cortex. Neuron 63:854–864
Stevenson RJ, Wilson DA (2007) Odour perception: an object-recognition approach. Perception 36:1821–1833
Takeuchi H, Ishida H, Hikichi S, Kurahashi T (2009) Mechanism of olfactory masking in the sensory cilia. J Gen Physiol 133:583–601
Tan J, Savigner A, Ma M, Luo M (2010) Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron 65:912–926
Thomas-Danguin T, Sinding C, Romagny S, El Mountassir F, Atanasova B, Le Berre E, Le Bon AM, Coureaud G (2014) The perception of odor objects in everyday life: a review on the processing of odor mixtures. Front Psychol 5:504. https://doi.org/10.3389/fpsyg.2014.00504
Urban NN, Sakmann B (2002) Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol 542:355–367
Vassar R, Chao SK, Sitcheran R, Nuñez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991
Weiss T, Snitz K, Yablonka A, Khan RM, Gafsou D, Schneidman E, Sobel N (2012) Perceptual convergence of multi-component mixtures in olfaction implies an olfactory white. Proc Natl Acad Sci 109:19959–19964
Wilson DA (2003) Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J Neurophysiol 90:65–72
Wilson DA, Stevenson RJ (2006) Learning to smell: olfactory perception from neurobiology to behavior. The Johns Hopkins University Press, Baltimore
Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519
Wilson RI, Mainen ZF (2006) Early events in olfactory processing. Annu Rev Neurosci 29:163–201
Wilson DA, Sullivan RM, Leon M (1987) Single-unit analysis of postnatal olfactory learning: modified olfactory bulb output response patterns to learned attractive odors. J Neurosci 7:3154–3162
Wiltrout C, Dogra S, Linster C (2003) Configurational and nonconfigurational interactions between odorants in binary mixtures. Behav Neurosci 117:236–245
Yamada Y, Bhaukaurally K, Madarász TJ, Pouget A, Rodriguez I, Carleton A (2017) Context- and output layer-dependent long-term ensemble plasticity in a sensory circuit. Neuron 93(1198–1212):e5
Yoshida I, Mori K (2007) Odorant category profile selectivity of olfactory cortex neurons. J Neurosci 27:9105–9114
Zarzo M, Stanton DT (2006) Identification of latent variables in a semantic odor profile database using principal component analysis. Chem Senses 31:713–724
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Murthy, V.N., Rokni, D. Processing of Odor Mixtures in the Mammalian Olfactory System. J Indian Inst Sci 97, 415–421 (2017). https://doi.org/10.1007/s41745-017-0045-1
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DOI: https://doi.org/10.1007/s41745-017-0045-1