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Human Olfaction: A Typical Yet Special Mammalian Olfactory System

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The Olfactory System

Abstract

In this chapter we concentrate on human olfaction, asking what the study of human olfaction has taught us about mammalian olfaction in general, and what it has shown as uniquely human olfactory structure and function. We first briefly highlight the superb olfactory capabilities of humans, starting with keen detection and discrimination, through unlikely tasks such as scent tracking, and culminating in complex social chemosignaling. We then describe the neural organization of human olfaction subserving these tasks, noting unique human olfactory sampling strategies, apparently unique organizational features of the human olfactory epithelium and bulb, and functional specializations in olfactory cortex. Although these attributes may constitute nuances of sensory system organization, the most unique aspect of human olfaction, and indeed of humans in general, remains coding into language. It is this language-based key that has allowed uncovering a small but significant portion of the rules by which molecular structures transform into olfactory percepts.

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References

  • Abolmaali ND, Kuhnau D, Knecht M, Kohler K, Huttenbrink KB, Hummel T (2001) Imaging of the human vomeronasal duct. Chem Senses 26:35–39

    PubMed  CAS  Google Scholar 

  • Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuro Endocrinol Lett 23:79–84

    PubMed  Google Scholar 

  • Albrecht J, Kopietz R, Frasnelli J, Wiesmann M, Hummel T, Lundstrom JN (2010) The neuronal correlates of intranasal trigeminal function: an ALE meta-analysis of human functional brain imaging data. Brain Res Rev 62:183–196

    PubMed Central  PubMed  Google Scholar 

  • Arzi A, Shedlesky L, Ben-Shaul M, Nasser K, Oksenberg A, Hairston IS, Sobel N (2012) Humans can learn new information during sleep. Nat Neurosci 15:1460–1465

    PubMed  CAS  Google Scholar 

  • Bell A (1914) Discovery and invention. Nat Geogr 25:649

    Google Scholar 

  • Bensafi M (2004) Sniffing a human sex-steroid derived compound affects mood and autonomic arousal in a dose-dependent manner. Psychoneuroendocrinology 29:1290–1299

    PubMed  CAS  Google Scholar 

  • Bensafi M, Porter J, Pouliot S, Mainland J, Johnson B, Zelano C, Young N, Bremner E, Aframian D, Khan R (2003a) Olfactomotor activity during imagery mimics that during perception. Nat Neurosci 6:1142–1144

    PubMed  CAS  Google Scholar 

  • Bensafi M, Brown WM, Tsutsui T, Mainland JD, Johnson BN, Bremner EA, Young N, Mauss I, Ray B, Gross J, Richards J, Stappen I, Levenson RW, Sobel N (2003b) Sex-steroid derived compounds induce sex-specific effects on autonomic nervous system function in humans. Behav Neurosci 117:1125–1134

    PubMed  CAS  Google Scholar 

  • Bensafi M, Brown WM, Khan R, Levenson B, Sobel N (2004) Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts. Behav Brain Res 152:11–22

    PubMed  CAS  Google Scholar 

  • Brennan PA (2001) The vomeronasal system. Cell Mol Life Sci 58:546–555

    PubMed  CAS  Google Scholar 

  • Buschhuter D, Smitka M, Puschmann S, Gerber JC, Witt M, Abolmaali ND, Hummel T (2008) Correlation between olfactory bulb volume and olfactory function. Neuroimage 42:498–502

    PubMed  CAS  Google Scholar 

  • Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346:403–434

    PubMed  CAS  Google Scholar 

  • Carnicelli V, Santoro A, Sellari-Franceschini S, Berrettini S, Zucchi R (2010) Expression of trace amine-associated receptors in human nasal mucosa. Chemosens Percept 3:99–107

    Google Scholar 

  • Castro JB, Ramanathan A, Chennubhotla CS (2013) Categorical dimensions of human odor descriptor space revealed by non-negative matrix factorization. PLoS One 8:e73289

    PubMed Central  PubMed  CAS  Google Scholar 

  • Cenier T, McGann JP, Tsuno Y, Verhagen JV, Wachowiak M (2013) Testing the sorption hypothesis in olfaction: a limited role for sniff strength in shaping primary odor representations during behavior. J Neurosci 33:79–92

    PubMed Central  PubMed  CAS  Google Scholar 

  • Cerda-Molina AL, Hernandez-Lopez L, de la OC, Chavira-Ramirez R, Mondragon-Ceballos R (2013) Changes in men’s salivary testosterone and cortisol levels, and in sexual desire after smelling female axillary and vulvar scents. Front Endocrinol (Lausanne) 4:159

    Google Scholar 

  • Cerf-Ducastel B, Murphy C (2006) Neural substrates of cross-modal olfactory recognition memory: an fMRI study. Neuroimage 31:386–396

    PubMed  Google Scholar 

  • Chen D, Haviland-Jones J (2000) Human olfactory communication of emotion. Percept Motor Skills 91:771

    PubMed  CAS  Google Scholar 

  • Chen D, Katdare A, Lucas N (2006) Chemosignals of fear enhance cognitive performance in humans. Chem Senses 31:415

    PubMed  CAS  Google Scholar 

  • Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WMC, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RLM, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249

    PubMed  CAS  Google Scholar 

  • Cutler WB, Preti G, Krieger A, Huggins GR, Garcia CR, Lawley HJ (1986) Human axillary secretions influence women’s menstrual cycles: the role of donor extract from men. Horm Behav 20:463–473

    PubMed  CAS  Google Scholar 

  • Dalton P, Doolittle N, Breslin PA (2002) Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci 5:199–200

    PubMed  CAS  Google Scholar 

  • de Groot JH, Semin GR, Smeets MA (2013) I can see, hear, and smell your fear: comparing olfactory and audiovisual media in fear communication. J Exp Psychol Gen 143:825–834

    PubMed  Google Scholar 

  • Deschenes M, Moore J, Kleinfeld D (2012) Sniffing and whisking in rodents. Curr Opin Neurobiol 22:243–250

    PubMed  CAS  Google Scholar 

  • Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T (2013) Non-redundant coding of aversive odours in the main olfactory pathway. Nature (Lond) 497:486–489

    CAS  Google Scholar 

  • Doty RL, Ford M, Preti G, Huggins GR (1975) Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science 190:1316–1318

    PubMed  CAS  Google Scholar 

  • Doty RL, Brugger WE, Jurs PC, Orndorff MA, Snyder PJ, Lowry LD (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol Behav 20:175–185

    PubMed  CAS  Google Scholar 

  • Dravnieks A (1985) Atlas of odor character profiles. ASTM Press, West Conshohocken

    Google Scholar 

  • Escada PA, Lima C, da Silva JM (2009) The human olfactory mucosa. Eur Arch Otorhinolaryngol 266:1675–1680

    PubMed  Google Scholar 

  • Ferdon S, Murphy C (2003) The cerebellum and olfaction in the aging brain: a functional magnetic resonance imaging study. Neuroimage 20:12–21

    PubMed  Google Scholar 

  • Feron F, Perry C, McGrath JJ, Mackay-Sim A (1998) New techniques for biopsy and culture of human olfactory epithelial neurons. Arch Otolaryngol Head Neck Surg 124:861–866

    PubMed  CAS  Google Scholar 

  • Frank RA, Dulay MF, Gesteland RC (2003) Assessment of the sniff magnitude test as a clinical test of olfactory function. Physiol Behav 78:195–204

    PubMed  CAS  Google Scholar 

  • Frasnelli J, Lundstrom JN, Boyle JA, Katsarkas A, Jones-Gotman M (2011) The vomeronasal organ is not involved in the perception of endogenous odors. Hum Brain Mapp 32:450–460

    PubMed Central  PubMed  Google Scholar 

  • Frumin I, Sobel N, Gilad Y (2013) Does a unique olfactory genome imply a unique olfactory world? Nat Neurosci 17:6–8

    Google Scholar 

  • Gabler S, Soelter J, Hussain T, Sachse S, Schmuker M (2013) Physicochemical vs. vibrational descriptors for prediction of odor receptor responses. Mol Inform 32:855–865

    CAS  Google Scholar 

  • Gelstein S, Yeshurun Y, Rozenkrantz L, Shushan S, Frumin I, Roth Y, Sobel N (2011) Human tears contain a chemosignal. Science 331:226–230

    PubMed  CAS  Google Scholar 

  • Gibbons B (1986) The intimate sense of smell. Nat Geogr 170:324–361

    Google Scholar 

  • Gilad Y, Lancet D (2003) Population differences in the human functional olfactory repertoire. Mol Biol Evol 20:307–314

    PubMed  CAS  Google Scholar 

  • Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11:628–641

    PubMed Central  PubMed  CAS  Google Scholar 

  • Gottfried JA, Winston JS, Dolan RJ (2006) Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49:467–479

    PubMed  CAS  Google Scholar 

  • Grosser BI, Monti-Bloch L, Jennings-White C, Berliner DL (2000) Behavioral and electrophysiological effects of androstadienone, a human pheromone. Psychoneuroendocrinology 25:289–299

    PubMed  CAS  Google Scholar 

  • Haddad R, Lapid H, Harel D, Sobel N (2008a) Measuring smells. Curr Opin Neurobiol 18:438–444

    PubMed  CAS  Google Scholar 

  • Haddad R, Khan R, Takahashi YK, Mori K, Harel D, Sobel N (2008b) A metric for odorant comparison. Nat Methods 5:425–429

    PubMed  CAS  Google Scholar 

  • Haddad R, Weiss T, Khan R, Nadler B, Mandairon N, Bensafi M, Schneidman E, Sobel N (2010) Global features of neural activity in the olfactory system form a parallel code that predicts olfactory behavior and perception. J Neurosci 30:9017–9026

    PubMed  CAS  Google Scholar 

  • Hauser R, Marczak M, Karaszewski B, Wiergowski M, Kaliszan M, Penkowski M, Kernbach-Wighton G, Jankowski Z, Namiesnik J (2008) A preliminary study for identifying olfactory markers of fear in the rat. Lab Anim (NY) 37:76–80

    Google Scholar 

  • Howard JD, Plailly J, Grueschow M, Haynes JD, Gottfried JA (2009) Odor quality coding and categorization in human posterior piriform cortex. Nat Neurosci 12:932–938

    PubMed Central  PubMed  CAS  Google Scholar 

  • Huart C, Rombaux P, Hummel T (2013) Plasticity of the human olfactory system: the olfactory bulb. Molecules 18:11586–11600

    PubMed  CAS  Google Scholar 

  • Hummel T, Livermore A (2002) Intranasal chemosensory function of the trigeminal nerve and aspects of its relation to olfaction. Int Arch Occup Environ Health 75:305–313

    PubMed  Google Scholar 

  • Hummel T, Mojet J, Kobal G (2006) Electro-olfactograms are present when odorous stimuli have not been perceived. Neurosci Lett 397:224–228

    PubMed  CAS  Google Scholar 

  • Hummer TA, McClintock MK (2009) Putative human pheromone androstadienone attunes the mind specifically to emotional information. Horm Behav 55:548–559

    PubMed  CAS  Google Scholar 

  • Ihara S, Yoshikawa K, Touhara K (2013) Chemosensory signals and their receptors in the olfactory neural system. Neuroscience 254:45–60

    PubMed  CAS  Google Scholar 

  • Ishimaru T, Reden J, Krone F, Scheibe M (2007) Optical recordings from the human nasal mucosa in response to olfactory stimulation. Neurosci Lett 423:231–235

    PubMed  CAS  Google Scholar 

  • Ishimaru T, Reden J, Krone F, Scheibe M (2011) Topographical differences in the sensitivity of the human nasal mucosa to olfactory and trigeminal stimuli. Neurosci Lett 493:136–139

    PubMed  CAS  Google Scholar 

  • Jacob S, Hayreh DJ, McClintock MK (2001a) Context-dependent effects of steroid chemosignals on human physiology and mood. Physiol Behav 74:15–27

    PubMed  CAS  Google Scholar 

  • Jacob S, Kinnunen LH, Metz J, Cooper M, McClintock MK (2001b) Sustained human chemosignal unconsciously alters brain function. Neuroreport 12:2391–2394

    PubMed  CAS  Google Scholar 

  • Jacob S, Spencer NA, Bullivant SB, Sellergren SA, Mennella JA, McClintock MK (2004) Effects of breastfeeding chemosignals on the human menstrual cycle. Hum Reprod 19:422–429

    PubMed  Google Scholar 

  • Johansson CB, Svensson M, Wallstedt L, Janson AM, Frisen J (1999) Neural stem cells in the adult human brain. Exp Cell Res 253:733–736

    PubMed  CAS  Google Scholar 

  • Johnson BN, Mainland JD, Sobel N (2003) Rapid olfactory processing implicates subcortical control of an olfactomotor system. J Neurophysiol 90:1084–1094

    PubMed  Google Scholar 

  • Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H (2007) Genetic variation in a human odorant receptor alters odour perception. Nature (Lond) 449:468–472

    CAS  Google Scholar 

  • Kermen F, Chakirian A, Sezille C, Joussain P, Le Goff G, Ziessel A, Chastrette M, Mandairon N, Didier A, Rouby C, Bensafi M (2011) Molecular complexity determines the number of olfactory notes and the pleasantness of smells. Sci Rep 1:206

    PubMed Central  PubMed  CAS  Google Scholar 

  • Keverne EB (1999) The vomeronasal organ. Science 286:716–720

    PubMed  CAS  Google Scholar 

  • Khan R, Luk C, 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

    PubMed  CAS  Google Scholar 

  • Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature (Lond) 437:898–901

    CAS  Google Scholar 

  • Kimoto H, Sato K, Nodari F, Haga S, Holy TE, Touhara K (2007) Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr Biol 17:1879–1884

    PubMed  CAS  Google Scholar 

  • Kjelvik G, Evensmoen HR, Brezova V, Haberg AK (2012) The human brain representation of odor identification. J Neurophysiol 108:645–657

    PubMed  Google Scholar 

  • Knaden M, Strutz A, Ahsan J, Sachse S, Hansson BS (2012) Spatial representation of odorant valence in an insect brain. Cell Rep 1:392–399

    PubMed  CAS  Google Scholar 

  • Knecht M, Hummel T (2004) Recording of the human electro-olfactogram. Physiol Behav 83:13–19

    PubMed  CAS  Google Scholar 

  • Knecht M, Lundstrom JN, Witt M, Huttenbrink KB, Heilmann S, Hummel T (2003) Assessment of olfactory function and androstenone odor thresholds in humans with or without functional occlusion of the vomeronasal duct. Behav Neurosci 117:1135–1141

    PubMed  Google Scholar 

  • Kobal G, Hummel T (1991) Human electro-olfactograms and brain responses to olfactory stimulation. In: Laing DG, Doty RL, Breipohl W (eds) The human sense of smell. Springer, Berlin

    Google Scholar 

  • Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature (Lond) 450:503–508

    CAS  Google Scholar 

  • Koulakov AA, Enikolopov AG, Rinberg D (2009) The structure of human olfactory space. Arxiv preprint arXiv:09073964

    Google Scholar 

  • Laing DG (1982) Characterisation of human behaviour during odour perception. Perception 11:221–230

    PubMed  CAS  Google Scholar 

  • Laing DG (1983) Natural sniffing gives optimum odour perception for humans. Perception 12:99–117

    PubMed  CAS  Google Scholar 

  • Lapid H, Hummel T (2013) Recording odor-evoked response potentials at the human olfactory epithelium. Chem Senses 38:3–17

    PubMed  Google Scholar 

  • Lapid H, Seo HS, Schuster B, Schneidman E, Roth Y, Harel D, Sobel N, Hummel T (2009) Odorant concentration dependence in electroolfactograms recorded from the human olfactory epithelium. J Neurophysiol 102:2121–2130

    PubMed  Google Scholar 

  • Lapid H, Shushan S, Plotkin A, Voet H, Roth Y, Hummel T, Schneidman E, Sobel N (2011) Neural activity at the human olfactory epithelium reflects olfactory perception. Nat Neurosci 14:1455–1461

    PubMed  CAS  Google Scholar 

  • Laska M, Freyer D (1997) Olfactory discrimination ability for aliphatic esters in squirrel monkeys and humans. Chem Senses 22:457–465

    PubMed  CAS  Google Scholar 

  • Laska M, Liesen A, Teubner P (1999a) Enantioselectivity of odor perception in squirrel monkeys and humans. Am J Physiol 277:R1098–R1103

    PubMed  CAS  Google Scholar 

  • Laska M, Trolp S, Teubner P (1999b) Odor structure-activity relationships compared in human and nonhuman primates. Behav Neurosci 113:998–1007

    PubMed  CAS  Google Scholar 

  • Leopold DA, Hummel T, Schwob JE, Hong SC, Knecht M, Kobal G (2000) Anterior distribution of human olfactory epithelium. Laryngoscope 110:417–421

    PubMed  CAS  Google Scholar 

  • 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

    PubMed Central  PubMed  CAS  Google Scholar 

  • Li W, Howard JD, Parrish TB, Gottfried JA (2008) Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319:1842–1845

    PubMed Central  PubMed  CAS  Google Scholar 

  • Li W, Lopez L, Osher J, Howard JD, Parrish TB, Gottfried JA (2010) Right orbitofrontal cortex mediates conscious olfactory perception. Psychol Sci 21:1454–1463

    PubMed Central  PubMed  Google Scholar 

  • Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature (Lond) 442:645–650

    CAS  Google Scholar 

  • Lundstrom JN, Olsson MJ (2005) Subthreshold amounts of social odorant affect mood, but not behavior, in heterosexual women when tested by a male, but not a female, experimenter. Biol Psychol 70:197–204

    PubMed  Google Scholar 

  • Madany Mamlouk A, Chee-Ruiter C, Hofmann UG, Bower JM (2003) Quantifying olfactory perception: mapping olfactory perception space by using multidimensional scaling and self-organizing maps. Neurocomputing 52:591–597

    Google Scholar 

  • Mainland JD, Bremner EA, Young N, Johnson BN, Khan RM, Bensafi M, Sobel N (2002) Olfactory plasticity: one nostril knows what the other learns. Nature (Lond) 419:802

    CAS  Google Scholar 

  • Mainland J, Johnson BN, Khan R, Ivry RB, Sobel N (2005) Olfactory impairments in patients with unilateral cerebellar lesions are selective to inputs from the contralesion nostril. J Neurosci 25:6362–6371

    PubMed  CAS  Google Scholar 

  • Mainland J, Keller A, Li Y, Zhou T, Trimmer C, Snyder L, Moberly A, Adipietro K, Liu W, Zhuang H, Zhan S, Lee S, Lin A, Matsunami H (2014) The missense of smell: functional variability in the human odorant receptor repertoire. Nat Neurosci 17:114–120

    PubMed  CAS  Google Scholar 

  • Mandairon N, Poncelet J, Bensafi M, Didier A (2009) Humans and mice express similar olfactory preferences. PLoS One 4:e4209

    PubMed Central  PubMed  Google Scholar 

  • Maresh A, Rodriguez Gil D, Whitman MC, Greer CA (2008) Principles of glomerular organization in the human olfactory bulb: implications for odor processing. PLoS One 3:e2640

    PubMed Central  PubMed  Google Scholar 

  • McClintock MK (1971) Menstrual synchrony and suppression. Nature (Lond) 229:244–245

    CAS  Google Scholar 

  • Menashe I, Abaffy T, Hasin Y, Goshen S, Yahalom V, Luetje CW, Lancet D (2007) Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol 5:e284

    PubMed Central  PubMed  Google Scholar 

  • Meredith M (2001) Human vomeronasal organ function: a critical review of best and worst cases. Chem Senses 26:433–445

    PubMed  CAS  Google Scholar 

  • Mozell MM, Jagodowicz M (1973) Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science 181:1247–1249

    PubMed  CAS  Google Scholar 

  • Mujica-Parodi LR, Strey HH, Frederick B, Savoy R, Cox D, Botanov Y, Tolkunov D, Rubin D, Weber J (2009) Chemosensory cues to conspecific emotional stress activate amygdala in humans. PLoS One 4:113–123

    Google Scholar 

  • Oh TJ, Kim MY, Park KS, Cho YM (2012) Effects of chemosignals from sad tears and postprandial plasma on appetite and food intake in humans. PLoS One 7:e42352

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pageat P, Gaultier E (2003) Current research in canine and feline pheromones. Vet Clin N Am Small Anim Pract 33:187–211

    Google Scholar 

  • Parthasarathy K, Bhalla US (2013) Laterality and symmetry in rat olfactory behavior and in physiology of olfactory input. J Neurosci 33:5750–5760

    PubMed  CAS  Google Scholar 

  • Plailly J, Howard JD, Gitelman DR, Gottfried JA (2008) Attention to odor modulates thalamocortical connectivity in the human brain. J Neurosci 28:5257–5267

    PubMed Central  PubMed  CAS  Google Scholar 

  • Porter J, Anand T, Johnson B, Khan RM, Sobel N (2005) Brain mechanisms for extracting spatial information from smell. Neuron 47:581–592

    PubMed  CAS  Google Scholar 

  • Porter J, Craven B, Khan RM, Chang SJ, Kang I, Judkewitz B, Volpe J, Settles G, Sobel N (2007) Mechanisms of scent-tracking in humans. Nat Neurosci 10:27–29

    PubMed  CAS  Google Scholar 

  • Prehn A, Ohrt A, Sojka B, Ferstl R, Pause BM (2006) Chemosensory anxiety signals augment the startle reflex in humans. Neurosci Lett 394:127–130

    PubMed  CAS  Google Scholar 

  • Prehn-Kristensen A, Wiesner C, Bergmann TO, Wolff S, Jansen O, Mehdorn HM, Ferstl R, Pause BM (2009) Induction of empathy by the smell of anxiety. PLoS One 4:e5987

    PubMed Central  PubMed  Google Scholar 

  • Price JL (1990) Olfactory system. In: Paxinos G (ed) The human nervous system. Academic Press, San Diego, pp 979–1001

    Google Scholar 

  • Qureshy A, Kawashima R, Imran MB, Sugiura M, Goto R, Okada K, Inoue K, Itoh M, Schormann T, Zilles K, Fukuda H (2000) Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol 84:1656–1666

    PubMed  CAS  Google Scholar 

  • Rajan R, Clement JP, Bhalla US (2006) Rats smell in stereo. Science 311:666–670

    PubMed  CAS  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597–609

    PubMed  CAS  Google Scholar 

  • Rojas-Libano D, Kay LM (2012) Interplay between sniffing and odorant sorptive properties in the rat. J Neurosci 32:15577–15589

    PubMed Central  PubMed  CAS  Google Scholar 

  • Royet JP, Zald D, Versace R, Costes N, Lavenne F, Koenig O, Gervais R (2000) Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. J Neurosci 20:7752–7759

    PubMed  CAS  Google Scholar 

  • Royet JP, Hudry J, Zald DH, Godinot D, Gregoire MC, Lavenne F, Costes N, Holley A (2001) Functional neuroanatomy of different olfactory judgments. Neuroimage 13:506–519

    PubMed  CAS  Google Scholar 

  • Russell MJ, Switz GM, Thompson K (1980) Olfactory influences on the human menstrual cycle. Pharmacol Biochem Behav 13:737–738

    PubMed  CAS  Google Scholar 

  • Sahay A, Wilson DA, Hen R (2011) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70:582–588

    PubMed Central  PubMed  CAS  Google Scholar 

  • Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD (2009) Odor coding by a mammalian receptor repertoire. Sci Signal 2:ra9

    PubMed Central  PubMed  Google Scholar 

  • Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature (Lond) 427:740–744

    CAS  Google Scholar 

  • Savic I, Gulyas B (2000) PET shows that odors are processed both ipsilaterally and contralaterally to the stimulated nostril. Neuroreport 11:2861–2866

    PubMed  CAS  Google Scholar 

  • Savic I, Berglund H, Gulyas B, Roland P (2001) Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31:661–668

    PubMed  CAS  Google Scholar 

  • Savic I, Berglund H, Lindstrom P (2005) Brain responses to putative pheromones in homosexual men. Proc Natl Acad Sci USA 102:7356–7361

    PubMed Central  PubMed  CAS  Google Scholar 

  • Scott J, Sherrill L, Jiang J, Zhao K (2014) Tuning to odor solubility and sorption pattern in olfactory epithelial responses. J Neurosci 34:2025–2036

    PubMed  CAS  Google Scholar 

  • Shanas U, Terkel J (1997) Mole-rat Harderian gland secretions inhibit aggression. Anim Behav 54:1255–1263

    PubMed  Google Scholar 

  • Shannahoff-Khalsa D (1991) Lateralized rhythms of the central and autonomic nervous systems. Int J Psychophysiol 11:225–251

    PubMed  CAS  Google Scholar 

  • Shepherd GM (2004) The human sense of smell: are we better than we think? PLoS Biol 2:E146

    PubMed Central  PubMed  Google Scholar 

  • Small DM, Gerber JC, Mak YE, Hummel T (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47:593–605

    PubMed  CAS  Google Scholar 

  • Snitz K, Yablonka A, Weiss T, Frumin I, Khan RM, Sobel N (2013) Predicting odor perceptual similarity from odor structure. PLoS Comput Biol 9:e1003184

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sobel N, Prabhakaran V, Hartley CA, Desmond JE, Zhao Z, Glover GH, Gabrieli JD, Sullivan EV (1998) Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci 18:8990–9001

    PubMed  CAS  Google Scholar 

  • Sobel N, Khan RM, Saltman A, Sullivan EV, Gabrieli JD (1999) The world smells different to each nostril. Nature (Lond) 402:35

    CAS  Google Scholar 

  • Stern K, McClintock MK (1998) Regulation of ovulation by human pheromones. Nature (Lond) 392:177–179

    CAS  Google Scholar 

  • Stoksted P (1953) Rhinometric measurements for determination of the nasal cycle. Acta Otolaryngol Suppl 109:159–175

    PubMed  CAS  Google Scholar 

  • Tham WW, Stevenson RJ, Miller LA (2009) The functional role of the mediodorsal thalamic nucleus in olfaction. Brain Res Rev 62:109–126

    PubMed  Google Scholar 

  • Trotier D (2011) Vomeronasal organ and human pheromones. Eur Ann Otorhinolaryngol Head Neck Dis 128:184–190

    PubMed  CAS  Google Scholar 

  • Trotier D, Eloit C, Wassef M, Talmain G, Bensimon JL, Doving KB, Ferrand J (2000) The vomeronasal cavity in adult humans. Chem Senses 25:369–380

    PubMed  CAS  Google Scholar 

  • Wang L, Chen L, Jacob T (2004) Evidence for peripheral plasticity in human odour response. J Physiol 554:236–244

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wang C, Liu F, Liu YY, Zhao CH, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21:1534–1550

    PubMed Central  PubMed  CAS  Google Scholar 

  • 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 USA 109:19959–19964

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519

    PubMed Central  PubMed  CAS  Google Scholar 

  • Witt M, Hummel T (2006) Vomeronasal versus olfactory epithelium: is there a cellular basis for human vomeronasal perception? Int Rev Cytol 248:209–259

    PubMed  CAS  Google Scholar 

  • Wu KN, Tan BK, Howard JD, Conley DB, Gottfried JA (2012) Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex. Nat Neurosci 15:1313–1319

    PubMed Central  PubMed  CAS  Google Scholar 

  • Wyart C, Webster WW, Chen JH, Wilson SR, McClary A, Khan RM, Sobel N (2007) Smelling a single component of male sweat alters levels of cortisol in women. J Neurosci 27:1261–1265

    PubMed  CAS  Google Scholar 

  • Wysocki CJ, Preti G (2004) Facts, fallacies, fears, and frustrations with human pheromones. Anat Rec A Discov Mol Cell Evol Biol 281:1201–1211

    PubMed  Google Scholar 

  • Wysocki CJ, Dorries KM, Beauchamp GK (1989) Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc Natl Acad Sci USA 86:7976–7978

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yeshurun Y, Sobel N (2010) An odor is not worth a thousand words: from multidimensional odors to unidimensional odor objects. Annu Rev Psychol 61:219–241

    PubMed  Google Scholar 

  • Young JM (2002) Different evolutionary processes shaped the mouse and human olfactory receptor gene families. Hum Mol Genet 11:535–546

    PubMed  CAS  Google Scholar 

  • Zarzo M (2008) Psychologic dimensions in the perception of everyday odors: pleasantness and edibility. J Sens Stud 23:354–376

    Google Scholar 

  • Zarzo M (2011) Hedonic judgments of chemical compounds are correlated with molecular size. Sensors (Basel) 11:3667–3686

    CAS  Google Scholar 

  • Zelano C, Sobel N (2005) Humans as an animal model for systems-level organization of olfaction. Neuron 48:431–454

    PubMed  CAS  Google Scholar 

  • Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133

    PubMed  CAS  Google Scholar 

  • Zhang J, Pacifico R, Cawley D, Feinstein P, Bozza T (2013) Ultrasensitive detection of amines by a trace amine-associated receptor. J Neurosci 33:3228–3239

    PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou W, Chen D (2009) Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychol Sci 20:177

    PubMed  Google Scholar 

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Weiss, T., Secundo, L., Sobel, N. (2014). Human Olfaction: A Typical Yet Special Mammalian Olfactory System. In: Mori, K. (eds) The Olfactory System. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54376-3_9

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