Habituation and adaptation to odors in humans

Habituation, or decreased behavioral response, to odors is created by repeated exposure and several detailed characteristics, whereas adaptation relates to the neural processes that constitute this decrease in a behavioral response. As with all senses, the olfactory system continually encounters an enormous variety of odorants which is why mechanisms must exist to segment them and respond to changes. Although most olfactory habitation studies have focused on animal models, this non-systematic review provides an overview of olfactory habituation and adaptation in humans, and techniques that have been used to measure them. Thus far, psychophysics in combination with modern techniques of neural measurement indicate that habituation to odors, or decrease of intensity, is relatively fast with adaptation occurring more quickly at higher cerebral processes than peripheral adaptation. Similarly, it has been demonstrated that many of the characteristics of habitation apply to human olfaction; yet, evidence for some characteristics such as potentiation of habituation or habituation of dishabituation need more support. Additionally, standard experimental designs should be used to minimize variance across studies, and more research is needed to define peripheral-cerebral feedback loops involved in decreased responsiveness to environmental stimuli.

[1]  Sanne Boesveldt,et al.  Signal-to-noise ratio of chemosensory event-related potentials , 2007, Clinical Neurophysiology.

[2]  T. Jacob,et al.  The correlation between physiological and psychological responses to odour stimulation in human subjects , 2002, Clinical Neurophysiology.

[3]  A. Kohn Visual adaptation: physiology, mechanisms, and functional benefits. , 2007, Journal of neurophysiology.

[4]  Adam Kepecs,et al.  Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making , 2006, Nature Reviews Neuroscience.

[5]  Artin Arshamian,et al.  A spatiotemporal comparison between olfactory and trigeminal event-related potentials , 2013, NeuroImage.

[6]  Fuqiang Zhao,et al.  Functional imaging of olfaction by CBV fMRI in monkeys: Insight into the role of olfactory bulb in habituation , 2015, NeuroImage.

[7]  Olfactory Detection Thresholds and Adaptation in Adults with Autism Spectrum Condition , 2012, Journal of autism and developmental disorders.

[8]  A. Steinemann,et al.  A review of a two-phase population study of multiple chemical sensitivities. , 2003, Environmental health perspectives.

[9]  A. Mouraux,et al.  Assessment of chemosensory function using electroencephalographic techniques. , 2012, Rhinology.

[10]  T. Hummel,et al.  Peripherally obtained electrophysiological responses to olfactory stimulation in man: electro-olfactograms exhibit a smaller degree of desensitization compared with subjective intensity estimates , 1996, Brain Research.

[11]  G Kobal,et al.  Chemosensory event-related potentials change with age. , 1998, Electroencephalography and clinical neurophysiology.

[12]  G. Arbanas Diagnostic and Statistical Manual of Mental Disorders (DSM-5) , 2015 .

[13]  Gerd Kobal,et al.  Differences in human chemosensory evoked potentials to olfactory and somatosensory chemical stimuli presented to left and right nostrils , 1992 .

[14]  D. G. Laing,et al.  Relationship between molecular structure, concentration and odor qualities of oxygenated aliphatic molecules. , 2003, Chemical senses.

[15]  S. Nordin,et al.  Prevalence and risk factors for self-reported odour intolerance: the Skövde population-based study , 2005, International archives of occupational and environmental health.

[16]  D. Wilson Olfaction as a model system for the neurobiology of mammalian short-term habituation , 2009, Neurobiology of Learning and Memory.

[17]  T. Hummel,et al.  Electro-Olfactograms in Humans in Response to Ortho- and Retronasal Chemosensory Stimulation , 2017, Chemosensory Perception.

[18]  R. Post Intermittent versus continuous stimulation: effect of time interval on the development of sensitization or tolerance. , 1980, Life sciences.

[19]  A novel psychophysical method for estimating the time course of olfactory rapid adaptation in humans. , 2010, Chemical senses.

[20]  T. Hummel,et al.  Chemo-somatosensory event-related potentials in response to repetitive painful chemical stimulation of the nasal mucosa. , 1994, Electroencephalography and clinical neurophysiology.

[21]  Herbert Stone,et al.  A comparison of olfactory adaptation among seven odorants and their relationship with several physicochemical properties , 1972 .

[22]  Ed. Aronsohn Experimentelle Untersuchungen zur Physiologie des Geruchs , 1888 .

[23]  T. Parrish,et al.  Learning to Smell the Roses: Experience-Dependent Neural Plasticity in Human Piriform and Orbitofrontal Cortices , 2006, Neuron.

[24]  C. Wysocki,et al.  Mutual cross-adaptation of the volatile steroid androstenone and a non-steroid perceptual analog , 1993 .

[25]  J. Covington,et al.  Olfactory event-related potentials: older males demonstrate the greatest deficits. , 1997, Electroencephalography and clinical neurophysiology.

[26]  Bruce R. Rosen,et al.  Activation and Habituation in Olfaction—An fMRI Study , 2001, NeuroImage.

[27]  C. Philpott,et al.  Olfactory clearance: what time is needed in clinical practice? , 2007, The Journal of Laryngology & Otology.

[28]  D. Wilson,et al.  Habituation of odor responses in the rat anterior piriform cortex. , 1998, Journal of neurophysiology.

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

[30]  Judith Gould,et al.  Describing the Sensory Abnormalities of Children and Adults with Autism , 2007, Journal of autism and developmental disorders.

[31]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[32]  A. Fairhall,et al.  Sensory adaptation , 2007, Current Opinion in Neurobiology.

[33]  J. Hildebrand,et al.  Olfactory information processing in the brain: encoding chemical and temporal features of odors. , 1996, Journal of neurobiology.

[34]  S. Nordin,et al.  Chemosensory perception, symptoms and autonomic responses during chemical exposure in multiple chemical sensitivity , 2015, International Archives of Occupational and Environmental Health.

[35]  T Lindvall,et al.  Perceived intensity of odor as a function of time of adaptation. , 1967, Scandinavian journal of psychology.

[36]  Debra F. McLaughlin,et al.  Evoked potentials as indices of adaptation in the somatosensory system in humans: A review and prospectus , 1993, Brain Research Reviews.

[37]  T. Kobayakawa,et al.  Effects of cognitive factors on perceived odor intensity in adaptation/habituation processes: from 2 different odor presentation methods. , 2007, Chemical senses.

[38]  S. Nordin,et al.  Chemosensory attention, habituation and detection in women and men. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  P. Dalton,et al.  Effects of long-term exposure to volatile irritants on sensory thresholds, negative mucosal potentials, and event-related potentials. , 2006, Behavioral neuroscience.

[40]  J. Harris,et al.  Habituatory response decrement in the intact organism. , 1943 .

[41]  F. Zufall,et al.  The cellular and molecular basis of odor adaptation. , 2000, Chemical senses.

[42]  Fred Rieke,et al.  Review the Challenges Natural Images Pose for Visual Adaptation , 2022 .

[43]  T. Hummel,et al.  Intranasal Odorant Concentrations in Relation to Sniff Behavior , 2014, Chemistry & biodiversity.

[44]  C. Wysocki,et al.  The role of perceptual and structural similarity in cross-adaptation. , 1996, Chemical senses.

[45]  David Cohen,et al.  What Can We Learn about Autism from Autistic Persons? , 2008, Psychotherapy and Psychosomatics.

[46]  W. Cain Bilateral interaction in olfaction , 1977, Nature.

[47]  C. M. Michel,et al.  Spatio–temporal dynamics of olfactory processing in the human brain: an event-related source imaging study , 2010, Neuroscience.

[48]  R R Neutra,et al.  Prevalence of people reporting sensitivities to chemicals in a population-based survey. , 1999, American journal of epidemiology.

[49]  Hadas Lapid,et al.  Recording odor-evoked response potentials at the human olfactory epithelium. , 2013, Chemical senses.

[50]  J. Gottfried Central mechanisms of odour object perception , 2010, Nature Reviews Neuroscience.

[51]  I. Croy,et al.  Habituation effects of pleasant and unpleasant odors. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  Antonio Schettino,et al.  rain mechanisms for emotional influences on perception and attention : hat is magic and what is not , 2012 .

[53]  C. Wysocki,et al.  Cross-adaptation of sweaty-smelling 3-methyl-2-hexenoic acid by a structurally-similar, pleasant-smelling odorant. , 1995, Chemical senses.

[54]  T. Jacob,et al.  Psychophysical evaluation of responses to pleasant and mal-odour stimulation in human subjects; adaptation, dose response and gender differences. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  C. Wysocki,et al.  The nature and duration of adaptation following long-term odor exposure , 1996, Perception & psychophysics.

[56]  T. Hummel,et al.  Time-course of trigeminal versus olfactory stimulation: evidence from chemosensory evoked potentials. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[57]  A. Keller,et al.  Humans Can Discriminate More than 1 Trillion Olfactory Stimuli , 2014, Science.

[58]  G Kobal,et al.  Cerebral chemosensory evoked potentials elicited by chemical stimulation of the human olfactory and respiratory nasal mucosa. , 1988, Electroencephalography and clinical neurophysiology.

[59]  Thomas Hummel,et al.  Subjective olfactory desensitization and recovery in humans. , 2014, Chemical senses.

[60]  T. Hummel,et al.  Olfactory function in patients with olfactory groove meningioma , 2001, Journal of neurology, neurosurgery, and psychiatry.

[61]  S. Schiffman,et al.  Science of odor as a potential health issue. , 2005, Journal of environmental quality.

[62]  P. Gagnon,et al.  Olfactory adaptation, threshold shift and recovery at low levels of exposure to methyl isobutyl ketone (MIBK). , 1994, Neurotoxicology.

[63]  J. White,et al.  Sniffing controls an adaptive filter of sensory input to the olfactory bulb , 2007, Nature Neuroscience.

[64]  J. Eggermont Peripheral auditory adaptation and fatigue: A model oriented review , 1985, Hearing Research.

[65]  David W. Smith,et al.  Evidence of rapid recovery from perceptual odor adaptation using a new stimulus paradigm , 2014, Attention, perception & psychophysics.

[66]  Peter Schieberle,et al.  Nature's chemical signatures in human olfaction: a foodborne perspective for future biotechnology. , 2014, Angewandte Chemie.

[67]  S. Nordin,et al.  Attention bias and sensitization in chemical sensitivity. , 2009, Journal of psychosomatic research.

[68]  Donald A Wilson,et al.  Olfactory cortical adaptation facilitates detection of odors against background. , 2006, Journal of neurophysiology.

[69]  T. Lorig,et al.  The application of electroencephalographic techniques to the study of human olfaction: a review and tutorial. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[70]  P. Groves,et al.  Habituation: a dual-process theory. , 1970, Psychological review.

[71]  M. Stuiver,et al.  Biophysics of the sense of smell , 1958 .

[72]  M. O'Mahony Salt Taste Adaptation: The Psychophysical Effects of Adapting Solutions and Residual Stimuli from Prior Tastings on the Taste of Sodium Chloride , 1979, Perception.

[73]  T. Hummel,et al.  New determinants of olfactory habituation , 2017, Scientific Reports.

[74]  J. C. Stevens,et al.  Olfactory Adaptation and Recovery in Old Age , 1989, Perception.

[75]  A. Mackay-Sim,et al.  Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects , 2007, European Archives of Oto-Rhino-Laryngology.

[76]  J. C. Stevens,et al.  Aging Speeds Olfactory Adaptation and Slows Recovery a , 1989 .

[77]  M. Webster,et al.  Visual adaptation: Neural, psychological and computational aspects , 2007, Vision Research.

[78]  Alison E. Lane,et al.  Sensory Processing Subtypes in Autism: Association with Adaptive Behavior , 2010, Journal of autism and developmental disorders.

[79]  D. Small,et al.  Differential Neural Responses Evoked by Orthonasal versus Retronasal Odorant Perception in Humans , 2005, Neuron.

[80]  H. Woodrow,et al.  A new olfactometric technique and some results , 1917 .

[81]  P. Dalton Psychophysical and behavioral characteristics of olfactory adaptation. , 2000, Chemical senses.

[82]  Herbert Stone,et al.  Changes in absolute detection threshold and in subjective intensity of suprathreshold stimuli during olfactory adaptation and recovery , 1970 .

[83]  G M Shepherd,et al.  Adaptive properties of olfactory receptors analysed with odour pulses of varying durations. , 1978, The Journal of physiology.

[84]  T. Hummel,et al.  Electro-olfactograms are present when odorous stimuli have not been perceived , 2006, Neuroscience Letters.

[85]  Noam Sobel,et al.  The sniff is part of the olfactory percept. , 2006, Chemical senses.

[86]  R. F. Thompson,et al.  Habituation: a model phenomenon for the study of neuronal substrates of behavior. , 1966, Psychological review.

[87]  Donald A. Wilson,et al.  Habituation revisited: An updated and revised description of the behavioral characteristics of habituation , 2009, Neurobiology of Learning and Memory.

[88]  L. Bennetto,et al.  Olfaction and Taste Processing in Autism , 2007, Biological Psychiatry.

[89]  G H Glover,et al.  Time course of odorant-induced activation in the human primary olfactory cortex. , 2000, Journal of neurophysiology.

[90]  Lars Muckli,et al.  Functional Magnetic Resonance Adaptation in Visual Neuroscience , 2008, Reviews in the neurosciences.

[91]  E. Donchin,et al.  On quantifying surprise: the variation of event-related potentials with subjective probability. , 1977, Psychophysiology.

[92]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[93]  H. Critchley,et al.  Impaired olfactory identification in Asperger's syndrome. , 2003, The Journal of neuropsychiatry and clinical neurosciences.

[94]  S. Solomon,et al.  Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons , 2014, Current Biology.

[95]  T. Hummel,et al.  Are there sex-related differences in responses to repetitive olfactory/trigeminal stimuli? , 2009, European Archives of Oto-Rhino-Laryngology.

[96]  C. Enroth-Cugell,et al.  Chapter 9 Visual adaptation and retinal gain controls , 1984 .

[97]  W. Cain,et al.  Olfactory adaptation as an aspect of odor similarity , 1992 .