Journal of Neurology

, Volume 264, Issue 4, pp 631–638 | Cite as

Olfaction as a marker for depression

Review

Abstract

Olfactory and emotional higher processing pathways share common anatomical substrates. Hence, depression is often accompanied by alterations in olfactory function. These alterations are negative in nature and may involve decreased activation in olfactory eloquent structures or decreased volume in the olfactory bulb (OB). We suggest that olfaction and depression interact in two ways. First, olfactory function in depression is impaired as a consequence of reduced olfactory attention and diminished olfactory receptor turnover rates. Second, the OB may constitute a marker for enhanced vulnerability to depression. Closer analysis of these interactions may help to explain observed experimental data, as well as to elucidate new therapeutic strategies involving olfaction. Because of the difficulties to disentangle cause from consequence in the relationship between olfaction and depression, longitudinal and intervention studies are necessary to elucidate this further.

Keywords

Nose Smell Flavor Olfactory bulb Depression 

Notes

Acknowledgments

We would like to acknowledge the support by the Deutsche Forschungsgemeinschaft to TH (DFG HU441/18-1).

Compliance with ethical standards

Conflicts of interest

None of the authors has a potential conflicts of interest.

References

  1. 1.
    Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:281–285CrossRefGoogle Scholar
  2. 2.
    Aschenbrenner K, Scholze N et al (2008) Gustatory and olfactory sensitivity in patients with anorexia and bulimia in the course of treatment. J Psychiatr Res 43(2):129–137CrossRefPubMedGoogle Scholar
  3. 3.
    Atanasova B, El-Hage W et al (2010) Olfactory anhedonia and negative olfactory alliesthesia in depressed patients. Psychiatry Res 176(2):190–196CrossRefPubMedGoogle Scholar
  4. 4.
    Bennetto L, Kuschner ES et al (2007) Olfaction and taste processing in autism. Biol Psychiatry 62(9):1015–1021CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Buschhuter D, Smitka M et al (2008) Correlation between olfactory bulb volume and olfactory function. Neuroimage 42(2):498–502CrossRefPubMedGoogle Scholar
  6. 6.
    Campbell S, Macqueen G (2004) The role of the hippocampus in the pathophysiology of major depression. J Psychiatry Neurosc 29(6):417–426Google Scholar
  7. 7.
    Clepce M, Gossler A, Reich K et al (2010) The relation between depression, anhedonia and olfactory hedonic estimates—a pilot study in major depression. Neurosci Lett 471(3):139–143CrossRefPubMedGoogle Scholar
  8. 8.
    Craig A (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13(4):500–505CrossRefPubMedGoogle Scholar
  9. 9.
    Croy I, Hummel T et al (2010) Quality of life following nasal surgery. Laryngoscope 120(4):826–831CrossRefPubMedGoogle Scholar
  10. 10.
    Croy I, Landis BN et al (2011) Patient adjustment to reduced olfactory function. Arch Otolaryngol Head Neck Surg 137(4):377–382CrossRefPubMedGoogle Scholar
  11. 11.
    Croy I, Negoias S et al (2012) Learning about the functions of the olfactory system from people without a sense of smell. PLoS One 7(3):e33365. doi: 10.31371/journal.pone.0033365 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Croy I, Negoias S et al (2013) Reduced olfactory bulb volume in adults with a history of childhood maltreatment. Chem Senses 38(8):679–684CrossRefPubMedGoogle Scholar
  13. 13.
    Croy I, Nordin S et al (2014) Olfactory disorders and quality of life–an updated review. Chem Senses 39(3):185–194CrossRefPubMedGoogle Scholar
  14. 14.
    Croy I, Olgun S et al. (2015) Peripheral adaptive filtering in human olfaction? Three studies on prevalence and effects of olfactory training in specific anosmia in more than 1600 participants. Cortex 73:180–187CrossRefPubMedGoogle Scholar
  15. 15.
    Croy I, Schulz M et al (2014) Human olfactory lateralization requires trigeminal activation. Neuroimage 98:289–295CrossRefPubMedGoogle Scholar
  16. 16.
    Croy I, Springborn M et al (2011) Agreeable smellers and sensitive neurotics—correlations among personality traits and sensory thresholds. PLoS One 6(4):e18701CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Croy I, Symmank A et al (2014) Olfaction as a marker for depression in humans. J Affect Disord 160:80–86CrossRefPubMedGoogle Scholar
  18. 18.
    Croy I, Yarina S et al (2013) Enhanced parosmia and phantosmia in patients with severe depression. Psychol Med 43(11):2460–2464CrossRefPubMedGoogle Scholar
  19. 19.
    Damasio A, Carvalho GB (2013) The nature of feelings: evolutionary and neurobiological origins. Nat Rev Neurosci 14(2):143–152CrossRefPubMedGoogle Scholar
  20. 20.
    Damm M, Pikart LK et al (2014) Olfactory training is helpful in postinfectious olfactory loss—a randomized controlled multicenter study. Laryngoscope 124:826–831CrossRefPubMedGoogle Scholar
  21. 21.
    de Groot JH, Smeets MA et al (2015) A sniff of happiness. Psychol Sci 26(6):684–700CrossRefPubMedGoogle Scholar
  22. 22.
    Deems DA, Doty RL et al (1991) Smell and taste disorders, a study of 750 patients from the University of Pennsylvania Smell and Taste Center. Arch Otolaryngol Head Neck Surg 117(5):519–528CrossRefPubMedGoogle Scholar
  23. 23.
    Ferdenzi C, Schaal B et al (2010) Family scents: developmental changes in the perception of kin body odor? J Chem Ecol 36(8):847–854CrossRefPubMedGoogle Scholar
  24. 24.
    Field T, Diego M et al (2005) Lavender fragrance cleansing gel effects on relaxation. Int J Neurosci 115:207–222CrossRefPubMedGoogle Scholar
  25. 25.
    Firestein S (2001) How the olfactory system makes sense of scents. Nature 413(6852):211–218CrossRefPubMedGoogle Scholar
  26. 26.
    Ganea K, Menke A et al (2012) Convergent animal and human evidence suggests the activin/inhibin pathway to be involved in antidepressant response. Transl Psychiatry 2:e177CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Gelstein S, Yeshurun Y et al (2011) Human tears contain a chemosignal. Science 331(6014):226–230CrossRefPubMedGoogle Scholar
  28. 28.
    Gottfried JA (2006) Smell: central nervous processing. Adv Otorhinolaryngol 63:44–69PubMedGoogle Scholar
  29. 29.
    Hawkes C (2003) Olfaction in neurodegenerative disorder. Mov Disord 18(4):364–372CrossRefPubMedGoogle Scholar
  30. 30.
    Hedner M, Larsson M et al (2010) Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol 30:1–6Google Scholar
  31. 31.
    Huart C, Rombaux P et al (2013) Plasticity of the human olfactory system: the olfactory bulb. Molecules 18(9):11586–11600. doi: 10.13390/molecules180911586 CrossRefPubMedGoogle Scholar
  32. 32.
    Hummel T, Rissom K et al (2009) Effects of olfactory training in patients with olfactory loss. Laryngoscope 119(3):496–499CrossRefPubMedGoogle Scholar
  33. 33.
    Hummel T, Smitka M et al (2011) Correlation between olfactory bulb volume and olfactory function in children and adolescents. Exp Brain Res 214(2):285–291CrossRefPubMedGoogle Scholar
  34. 34.
    Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex. Brain Res Rev 56(1):27–78CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Keller A (2011) Attention and olfactory consciousness. Front Psychol 2:380CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Kelly JP, Wrynn AS et al (1997) The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 74:299–316CrossRefPubMedGoogle Scholar
  37. 37.
    Kiecolt-Glaser JK, Graham JE et al (2008) Olfactory influences on mood and autonomic, endocrine, and immune function. Psychoneuroendocrinology 33:328–339CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Koenigs M, Grafman J (2009) The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behav Brain Res 201(1):239–243CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Komori T, Fujiwara R et al (1995) Effects of citrus fragrance on immune function and depressive states. Neuroimmunomodulation 2(3):174–180CrossRefPubMedGoogle Scholar
  40. 40.
    Kopala LC, Good KP, Honer WG (1994) Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophr Res 12(3):205–211CrossRefPubMedGoogle Scholar
  41. 41.
    Krajnik J, Kollndorfer K et al (2014) The impact of olfactory dysfunction on interoceptive awareness. PsychophysiologyGoogle Scholar
  42. 42.
    Lapid H, Shushan S et al (2011) Neural activity at the human olfactory epithelium reflects olfactory perception. Nat Neurosci 14:1455–1461CrossRefPubMedGoogle Scholar
  43. 43.
    Lascano AM, Hummel T et al (2010) Spatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study. Neuroscience 167:700–708CrossRefPubMedGoogle Scholar
  44. 44.
    LeDoux J (2012) Rethinking the emotional brain. Neuron 73(4):653–676. doi: 10.1016/j.neuron.2012.02.004 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Lehrner J, Eckersberger C et al (2000) Ambient odor of orange in 1540 a dental office reduces anxiety and improves mood in female patients. Physiol Behav 71:83–86CrossRefPubMedGoogle Scholar
  46. 46.
    Leonard BE (1984) The olfactory bulbectomized rat as a model of depression. Pol J Pharmacol Pharm 36:561–569PubMedGoogle Scholar
  47. 47.
    Li Q, Yang D et al (2015) Reduced amount of olfactory receptor neurons in the rat model of depression. Neurosci Lett 603:48–54CrossRefPubMedGoogle Scholar
  48. 48.
    Lombion-Pouthier S, Vandel P et al (2006) Odor perception in patients with mood disorders. J Affect Disord 90(2–3):187–191CrossRefPubMedGoogle Scholar
  49. 49.
    Lotsch J, Reichmann H et al (2008) Different odor tests contribute differently to the evaluation of olfactory loss. Chem Senses 33(1):17–21CrossRefPubMedGoogle Scholar
  50. 50.
    Lotsch J, Schaeffeler E et al (2014) Functional genomics suggest neurogenesis in the adult human olfactory bulb. Brain Struct Funct 219(6):1991–2000CrossRefPubMedGoogle Scholar
  51. 51.
    Lübke KT, Croy I et al (2014) Does human body odor represent a significant and rewarding social signal to individuals high in social openness? PLoS One 9(4):e94314CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Lundström JN, Mathe A et al (2013) Cerebral responses to the body odor of newborns are modulated by maternal status. Front PsycholGoogle Scholar
  53. 53.
    MacLean PD (1949) Psychosomatic disease and the “visceral brain”: recent developments bearing on the Papez theory of emotion. Psychosom Med 11(6):338–353CrossRefPubMedGoogle Scholar
  54. 54.
    Masini CV, Holmes PV et al (2004) Dopamine overflow is increased in olfactory bulbectomized rats: an in vivo microdialysis study. Physiol Behav 81(1):111–119CrossRefPubMedGoogle Scholar
  55. 55.
    Moberg PJ, Agrin R et al (1999) Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 21(3):325–340CrossRefPubMedGoogle Scholar
  56. 56.
    Mueller A, Rodewald A et al (2005) Reduced olfactory bulb volume in post-traumatic and post-infectious olfactory dysfunction. Neuroreport 16(5):475–478CrossRefPubMedGoogle Scholar
  57. 57.
    Naudin M, Atanasova B (2014) Olfactory markers of depression and Alzheimer’s disease. Neurosci Biobehav Rev 45:262–270CrossRefGoogle Scholar
  58. 58.
    Naudin M, Carl T et al (2014) Perceptive biases in major depressive episode. PLoS One 9(2):e86832CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Naudin M, El-Hage W et al (2012) State and trait olfactory markers of major depression. PLoS One 7(10):e46938CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Negoias S, Croy I et al (2010) Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience 169(1):415–421CrossRefPubMedGoogle Scholar
  61. 61.
    Negoias S, Hummel T, Symmank A, Schellong J, Joraschky P, Croy I (2016) Olfactory bulb volume predicts therapeutic outcome in major depression disorder. Brain Imaging Behav 10:367–372CrossRefPubMedGoogle Scholar
  62. 62.
    Nestler EJ, Barrot M et al (2002) Neurobiology of depression. Neuron 34(1):13–25CrossRefPubMedGoogle Scholar
  63. 63.
    Northcutt RG (2002) Understanding vertebrate brain evolution. Integr Comp Biol 42(4):743–756CrossRefPubMedGoogle Scholar
  64. 64.
    O’Doherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14(6):769–776CrossRefPubMedGoogle Scholar
  65. 65.
    Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206–219CrossRefPubMedGoogle Scholar
  66. 66.
    Oral E, Aydin MD et al (2013) How olfaction disorders can cause depression? The role of habenular degeneration. Neuroscience 240:63–69CrossRefPubMedGoogle Scholar
  67. 67.
    Paulus MP, Stein MB (2010) Interoception in anxiety and depression. Brain Struct Funct 214(5–6):451–463CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Pause BM, Miranda A et al (2001) Reduced olfactory performance in patients with major depression. J Psychiatr Res 35(5):271–277CrossRefPubMedGoogle Scholar
  69. 69.
    Pause BM, Raack N et al (2003) Convergent and divergent effects of odors and emotions in depression. Psychophysiology 40(2):209–225CrossRefPubMedGoogle Scholar
  70. 70.
    Pentzek M, Grass-Kapanke B, Ihl R (2007) Odor identification in Alzheimer’s disease and depression. Aging Clin Exp Res 19(3):255–258CrossRefPubMedGoogle Scholar
  71. 71.
    Pollatos O, Albrecht J et al (2007) Reduced olfactory sensitivity in subjects with depressive symptoms. J Affect Disord 102(1):101–108CrossRefPubMedGoogle Scholar
  72. 72.
    Porter RH, Moore JD (1981) Human kin recognition by olfactory cues. Physiol Behav 27(3):493–495CrossRefPubMedGoogle Scholar
  73. 73.
    Postolache TT, Doty RL et al (1999) Monorhinal odor identification and depression scores in patients with seasonal affective disorder. J Affect Disord 56(1):27–35CrossRefPubMedGoogle Scholar
  74. 74.
    Prehn-Kristensen A, Wiesner C et al (2009) Induction of empathy by the smell of anxiety. PLoS One 4(6):e5987CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Pribram KH, Kruger L (1954) Functions of the “olfactory brain”. Ann N Y Acad Sci 58(2):109–138CrossRefPubMedGoogle Scholar
  76. 76.
    Rossi M, Perez-Lloret S et al (2015) Olfactory dysfunction evaluation is not affected by comorbid depression in Parkinson’s disease. Mov Disord 30(9):1275–1279CrossRefPubMedGoogle Scholar
  77. 77.
    Rowe TB, Macrini TE et al (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):955–957CrossRefPubMedGoogle Scholar
  78. 78.
    Schriever VA, Lehmann S et al (2014) Preventing olfactory deterioration: olfactory training may be of help in older people. J Am Geriatr Soc 62(2):384–386CrossRefPubMedGoogle Scholar
  79. 79.
    Scinska A, Sienkiewicz-Jarosz H et al (2008) Depressive symptoms and olfactory function in older adults. Psychiatry Clin Neurosci 62(4):450–456CrossRefPubMedGoogle Scholar
  80. 80.
    Sela L, Sobel N (2010) Human olfaction: a constant state of change-blindness. Exp Brain Res 205(1):13–29CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Serby M, Larson P, Kalkstein D (1990) Olfactory sense in psychoses. Biol Psychiatry 28(9):830CrossRefPubMedGoogle Scholar
  82. 82.
    Soares JC, Mann JJ (1997) The functional neuroanatomy of mood disorders. J Psychiatr Res 31:393–432CrossRefPubMedGoogle Scholar
  83. 83.
    Song C, Leonard BE (2005) The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 29(4–5):627–647CrossRefPubMedGoogle Scholar
  84. 84.
    Stevenson RJ (2010) An initial evaluation of the functions of human olfaction. Chem Senses 35(1):3–20CrossRefPubMedGoogle Scholar
  85. 85.
    Swiecicki L, Zatorski P et al (2009) Gustatory and olfactory function in patients with unipolar and bipolar depression. Prog Neuropsychopharmacol Biol Psychiatry 33(5):827–834CrossRefPubMedGoogle Scholar
  86. 86.
    Temmel AF, Quint C et al (2002) Characteristics of olfactory disorders in relation to major causes of olfactory loss. Arch Otolaryngol Head Neck Surg 128(6):635–641CrossRefPubMedGoogle Scholar
  87. 87.
    Urretavizcaya M, Moreno I et al (2003) Auditory event-related potentials in 50 melancholic patients: increased N100, N200 and P300 latencies and diminished P300 amplitude. J Affect Disord 74(3):293–297CrossRefPubMedGoogle Scholar
  88. 88.
    Wang L, Chen L, Jacob T (2004) Evidence for peripheral plasticity in human odour response. J Physiol 554:236–244CrossRefPubMedGoogle Scholar
  89. 89.
    Warner MD, Peabody CA, Csernansky JG (1990) Olfactory functioning in schizophrenia and depression. Biol Psychiatry 27(4):457–458CrossRefPubMedGoogle Scholar
  90. 90.
    Wegener B-A, Croy I et al (2015) Olfactory training with older people. Chemical senses. Oxford University Press, OxfordGoogle Scholar
  91. 91.
    Wilson DA, Chapuis J et al (2015) Cortical olfactory anatomy and physiology. In: Doty RL (ed) Handbook of olfactioon and gustation, 3rd edn. Wiley, Hoboken, pp 209–223CrossRefGoogle Scholar
  92. 92.
    Winston JS, Gottfried JA, Kilner JM, Dolan RJ (2005) Integrated neural representations of odor intensity and affective valence in human amygdala. J Neurosci 28:8903–8907CrossRefGoogle Scholar
  93. 93.
    Yousem D, Geckle R et al (1996) MR evaluation of patients with congenital hyposmia or anosmia. Am J Roentgenol 166(2):439–443CrossRefGoogle Scholar
  94. 94.
    Yousem DM, Geckle RJ et al (1999) Posttraumatic smell loss: relationship of psychophysical tests and volumes of the olfactory bulbs and tracts and the temporal lobes. Acad Radiol 6:264–272CrossRefPubMedGoogle Scholar
  95. 95.
    Zald DH, Pardo JV (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 15:4119–4124CrossRefGoogle Scholar
  96. 96.
    Zucco GM, Bollini F (2011) Odour recognition memory and odour identification in patients with mild and severe major depressive disorders. Psychiatry Res 190(2):217–220CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Psychotherapy and Psychosomatic Medicine, Carl Gustav Carus Faculty of MedicineTechnische Universität DresdenDresdenGermany
  2. 2.Department of Otorhinolaryngology, Smell and Taste Clinic, Carl Gustav Carus Faculty of MedicineTechnische Universität DresdenDresdenGermany

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