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Different Brain Activation in Response to Repeated Odors of Pleasantness and Unpleasantness

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Chemosensory Perception

Abstract

Introduction

Brain activation in response to olfactory stimuli has been studied using functional magnetic resonance imaging (fMRI), but there is little knowledge about processing repeated olfactory information which is usual in daily life.

Methods

This fMRI study was designed to investigate brain response to repeated odorant stimulation with positive and negative valences in 12 healthy right-handed volunteers. There was a 25-min rest interval between two fMRI runs with identical stimulation paradigms with two odors, as phenylethyl alcohol (PEA) and isovaleric acid (IVA), and the two odors were released alternately.

Results

There was a similar activation pattern in regions of primary and secondary olfactory cortex induced by odors of both valences, especially by negative odor. Weakened activation of the brain is responsive to repeated both pleasant and unpleasant smell. Nevertheless, the repeated unpleasant odor has a more intimate relationship with the piriform cortex, amygdala, and hippocampus.

Conclusion

We conclude that asymmetric brain activation in response to repeated odorant stimulation depended on valences and that the unpleasant odor can evoke more negative emotion and profound memory.

Implications

We explore the central processing about repeated olfactory information applied fMRI for the first time, revealing asymmetric brain activation in response to repeated odors of pleasantness and unpleasantness.

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References

  • Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JDE, Sobel N (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6(2):196–202

    Article  CAS  PubMed  Google Scholar 

  • Arshamian A, Iannilli E, Gerber JC, Willander J, Persson J, Seo HS, Hummel T, Larsson M (2013) The functional neuroanatomy of odor evoked autobiographical memories cued by odors and words. Neuropsychologia 51(1):123–131

    Article  PubMed  Google Scholar 

  • Bensafi M, Sobel N, Khan RM (2007) Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. J Neurophysiol 98(6):3254–3262

    Article  PubMed  Google Scholar 

  • Bensafi M, Iannilli E, Poncelet J, Seo HS, Gerber J, Rouby C, Hummel T (2012) Dissociated representations of pleasant and unpleasant olfacto-trigeminal mixtures: an FMRI study. PLoS One 7(6):e38358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berlin HA, Stern ER, Ng J, Zhang S, Rosenthal D, Turetzky R et al (2017) Altered olfactory processing and increased insula activity in patients with obsessive-compulsive disorder: an fMRI study. Psychiatry Res 262:15–24

    Article  PubMed Central  Google Scholar 

  • Boesveldt S, Frasnelli J, Gordon AR, Lundström JN (2010) The fish is bad: negative food odors elicit faster and more accurate reactions than other odors. Biol Psychol 84(2):313–317

    Article  CAS  PubMed  Google Scholar 

  • Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346(3):403–434

    Article  CAS  PubMed  Google Scholar 

  • Ferdenzi C, Poncelet J, Rouby C, Bensafi M (2014) Repeated exposure to odors induces affective habituation of perception and sniffing. Front Behav Neurosci 8:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Fjaeldstad A, Fernandes HM, Van Hartevelt TJ, Gleesborg C, Møller A, Ovesen T et al (2017) Brain fingerprints of olfaction: a novel structural method for assessing olfactory cortical networks in health and disease. Sci Rep 7:42534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fulbright RK, Skudlarski P, Lacadie CM, Warrenburg S, Bowers AA, Gore JC et al (1998) Functional MR imaging of regional brain responses to pleasant and unpleasant odors. AJNR Am J Neuroradiol 19(9):1721–1726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghio M, Schulze P, Suchan B, Bellebaum C (2016) Neural representations of novel objects associated with olfactory experience. Behav Brain Res 308:143–151

    Article  PubMed  Google Scholar 

  • Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Brain Res Rev 50(2):287–304

    Article  PubMed  Google Scholar 

  • Gottfried JA, Deichmann R, Winston JS, Dolan RJ (2002) Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci 22(24):10819–10828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottfried JA, Smith AP, Rugg MD, Dolan RJ (2004) Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron 42(4):687–695

    Article  CAS  PubMed  Google Scholar 

  • Grabenhorst F, Rolls ET, Margot C, da Silva MA, Velazco MI (2007) How pleasant and unpleasant stimuli combine in different brain regions: odor mixtures. J Neurosci 27(49):13532–13540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hummel T, Knecht M, Kobal G (1996) Peripherally obtained electrophysiological responses to olfactory stimulation in man: electro-olfactograms exhibit a smaller degree of desensitization compared with subjective intensity estimates. Brain Res 717(1–2):160–164

    Article  CAS  PubMed  Google Scholar 

  • Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22(1):39–52

    Article  CAS  PubMed  Google Scholar 

  • Hummel T, Mojet J, Kobal G (2006) Electro-olfactograms are present when odorous stimuli have not been perceived. Neurosci Lett 397(3):224–228

    Article  CAS  PubMed  Google Scholar 

  • Hummel T, Fark T, Baum D, Warr J, Hummel CB, Schriever VA (2017) The rewarding effect of pictures with positive emotional connotation upon perception and processing of pleasant odors-an FMRI study. Front Neuroanat 11:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin J, Zelano C, Gottfried JA, Mohanty A (2015) Human amygdala represents the complete spectrum of subjective valence. J Neurosci 35(45):15145–15156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karunanayaka PR, Wilson DA, Vasavada M, Wang J, Martinez B, Tobia MJ et al (2015) Rapidly acquired multisensory association in the olfactory cortex. Brain Behav 5(11):e00390

    Article  PubMed  PubMed Central  Google Scholar 

  • Katata K, Sakai N, Doi K, Kawamitsu H, Fujii M, Sugimura K et al (2009) Functional MRI of regional brain responses to ‘pleasant’ and ‘unpleasant’ odors. Acta Otolaryngol Suppl 562:85–90

    Article  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    Article  CAS  PubMed  Google Scholar 

  • Li W (2014) Learning to smell danger: acquired associative representation of threat in the olfactory cortex. Front Behav Neurosci 8:98

    PubMed  PubMed Central  Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19(3):1233–1239

    Article  PubMed  Google Scholar 

  • McDonald AJ, Mott DD (2017) Functional neuroanatomy of amygdalohippocampal interconnections and their role in learning and memory. J Neurosci Res 95(3):797–820

    Article  CAS  PubMed  Google Scholar 

  • Patin A, Pause BM (2015) Human amygdala activations during nasal chemoreception. Neuropsychologia 78:171–194

    Article  PubMed  Google Scholar 

  • Pellegrino R, Sinding C, de Wijk RA, Hummel T (2017) Habituation and adaptation to odors in humans. Physiol Behav 177:13–19

    Article  CAS  PubMed  Google Scholar 

  • Philpott CM, Wolstenholme CR, Goodenough PC, Clark A, Murty GE (2008) Olfactory clearance: what time is needed in clinical practice. J Laryngol Otol 122(9):912–917

    Article  CAS  PubMed  Google Scholar 

  • Plailly J, Howard JD, Gitelman DR, Gottfried JA (2008) Attention to odor modulates thalamocortical connectivity in the human brain. J Neurosci 28(20):5257–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reichert JL, Ninaus M, Schuehly W, Hirschmann C, Bagga D, Schöpf V (2017) Functional brain networks during picture encoding and recognition in different odor contexts. Behav Brain Res 333:98–108

    Article  CAS  PubMed  Google Scholar 

  • Rolls ET, Kringelbach ML, de Araujo IE (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci 18(3):695–703

    Article  PubMed  Google Scholar 

  • Royet JP, Plailly J, Delon-Martin C, Kareken DA, Segebarth C (2003) fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender. NeuroImage 20(2):713–728

    Article  PubMed  Google Scholar 

  • Royet JP, Morin-Audebrand L, Cerf-Ducastel B, Haase L, Issanchou S, Murphy C, Fonlupt P, Sulmont-Rossé C, Plailly J (2011) True and false recognition memories of odors induce distinct neural signatures. Front Hum Neurosci 5:65

    Article  PubMed  PubMed Central  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(4):593–605

    Article  CAS  PubMed  Google Scholar 

  • Sobel N, Prabhakaran V, Zhao Z, Desmond JE, Glover GH, Sullivan EV, Gabrieli JDE (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol 83(1):537–551

    Article  CAS  PubMed  Google Scholar 

  • Stuck BA, Fadel V, Hummel T, Sommer JU (2014) Subjective olfactory desensitization and recovery in humans. Chem Senses 39(2):151–157

    Article  CAS  PubMed  Google Scholar 

  • Tham WW, Stevenson RJ, Miller LA (2011) The role of the mediodorsal thalamic nucleus in human olfaction. Neurocase 17(2):148–159

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Eslinger PJ, Smith MB, Yang QX (2005) Functional magnetic resonance imaging study of human olfaction and normal aging. J Gerontol A Biol Sci Med Sci 60(4):510–514

    Article  PubMed  Google Scholar 

  • Zatorre RJ, Jones-Gotman M, Rouby C (2000) Neural mechanisms involved in odor pleasantness and intensity judgments. Neuroreport 11(12):2711–2716

    Article  CAS  PubMed  Google Scholar 

  • Zelano C, Montag J, Johnson B, Khan R, Sobel N (2007) Dissociated representations of irritation and valence in human primary olfactory cortex. J Neurophysiol 97(3):1969–1976

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Key Research and Development Program of China (2016YFC0800700) and Beijing Key Laboratory of upper airway dysfunction related cardiovascular diseases (BZ0377).

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Correspondence to Yongxiang Wei.

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The authors declare that they have no conflict of interest.

Ethical Approval

The study has been approved by the local ethics committee and was conducted according to the Declaration of Helsinki on Biomedical Research Involving Human Subjects.

Informed Consent

Subjects were given detailed information about all testing procedures during enrollment. Written informed consent was obtained from all subjects before their participation.

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Xiao, W., Lv, Q., Gao, X. et al. Different Brain Activation in Response to Repeated Odors of Pleasantness and Unpleasantness. Chem. Percept. 13, 84–91 (2020). https://doi.org/10.1007/s12078-019-09270-y

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  • DOI: https://doi.org/10.1007/s12078-019-09270-y

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