- freely available
Brain Sci. 2016, 6(3), 22; doi:10.3390/brainsci6030022
2. Odor-Evoked Memory and Psychological Responses
3. Odor-Evoked Memory and Physiological Responses
4. Issues for Consideration
4.1. Odor Perception
4.2. Experience and Genetics
4.3. Gender and Age
Conflicts of Interest
- Engen, T. The Perception of Odors; Academic Press: Toronto, ON, Canada, 1982.
- Herz, R.S. Odor-evoked memory. In The Oxford Handbook of Social Neuroscience; Decety, J., Cacioppo, J., Eds.; Oxford University Press: New York, NY, USA, 2011; pp. 265–276.
- Herz, R.S.; Engen, T. Odor memory: Review and analysis. Psychon. Bull. Rev. 1996, 3, 300–313. [CrossRef] [PubMed]
- Pinto, J.M.; Wroblewski, K.E.; Kern, D.W.; Schumm, L.P.; McClintock, M.K. Olfactory dysfunction predicts 5-year mortality in older adults. PLoS ONE 2014, 9, e107541. [CrossRef] [PubMed]
- Doty, R.L. Olfaction in Parkinson’s disease and related disorders. Neurobiol. Dis. 2012, 46, 527–552. [CrossRef] [PubMed]
- Velayudhan, L. Smell identification function and Alzheimer’s disease: A selective review. Curr. Opin. Psychiatry 2015, 28, 173–179. [PubMed]
- Jellinek, J.S. Proust remembered: Has Proust’s account of odor-cue autobiographical memory recall really been investigated? Chem. Sens. 2004, 29, 455–458. [CrossRef] [PubMed]
- Proust, M. Swann’s Way; Modern Library: New York, NY, USA, 1928.
- Larsson, M.; Willander, J.; Karlsson, K.; Arshamian, A. Olfactory LOVER: Behavioral and neural correlates of autobiographical odor memory. Front. Psychol. 2014, 5, 312. [CrossRef] [PubMed]
- Chu, S.; Downes, J.J. Long live Proust: The odour-cued autobiographical memory bump. Cognition 2000, 75, 41–50. [CrossRef]
- Rubin, D.C.; Groth, E.; Goldsmith, D.J. Olfactory cueing of autobiographical memory. Am. J. Psychol. 1984, 97, 493–507. [CrossRef] [PubMed]
- Willander, J.; Larsson, M. Smell your way back to childhood: Autobiographical odor memory. Psychon. Bull. Rev. 2006, 13, 240–244. [CrossRef] [PubMed]
- Miles, A.N.; Berntsen, D. Odour-induced mental time travel into the past and future: Do odour cues retain a unique link to our distant past? Memory 2011, 19, 930–940. [CrossRef] [PubMed]
- Arshamian, A.; Iannilli, E.; Gerber, J.C.; Willander, J.; Persson, J.; Seo, H.S.; Larsson, M. The functional neuroanatomy of odor-evoked autobiographical memories cued by odors and ords. Neuropsychologia 2013, 51, 123–131. [CrossRef] [PubMed]
- Herz, R.S. Are odors the best cues to memory? A cross-modal comparison of associative memory stimuli. Ann. N. Y. Acad. Sci. 1998, 855, 670–674. [CrossRef] [PubMed]
- Herz, R.S. A naturalistic analysis of autobiographical memories triggered by olfactory, visual and auditory stimuli. Chem. Sens. 2004, 29, 217–224. [CrossRef]
- Herz, R.S.; Cupchik, G.C. The emotional distinctiveness of odor-evoked memories. Chem. Sens. 1995, 20, 517–528. [CrossRef]
- Herz, R.S.; Eliassen, J.C.; Beland, S.L.; Souza, T. Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia 2004, 42, 371–378. [CrossRef] [PubMed]
- Herz, R.S.; Schooler, J.W. A naturalistic study of autobiographical memories evoked to olfactory versus visual cues. Am. J. Psychol. 2002, 115, 21–32. [CrossRef] [PubMed]
- Willander, J.; Larsson, M. Olfaction and emotion: The case of autobiographical memory. Mem. Cognit. 2007, 35, 1659–1663. [CrossRef] [PubMed]
- Aggleton, J.P.; Mishkin, M. The amygdala: Sensory gateway to the emotions. In Emotion: Theory, Research and Experience, Volume 3: Biological Foundations of Emotion; Plutchik, R., Ellerman, H., Eds.; Academic Press: Orlando, FL, USA, 1986; pp. 281–299.
- Cahill, L.; Babinsky, R.; Markowitsch, H.J.; McGaugh, J.L. The amygdala and emotional memory. Nature 1995, 377, 295–296. [CrossRef] [PubMed]
- Eichenbaum, H. The hippocampus and declarative memory: Cognitive mechanisms and neural codes. Behav. Brain Res. 2001, 127, 199–207. [CrossRef]
- Turner, B.H.; Mishkin, M.; Knapp, M. Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol. 1980, 191, 515–543. [CrossRef] [PubMed]
- Davidson, R.J.; Putnam, K.M.; Larson, C.L. Dysfunction in the neural circuitry of emotion regulation—A possible prelude to violence. Science 2000, 289, 591–594. [CrossRef] [PubMed]
- Quirk, G.J.; Gehlert, D.R. Inhibition of the amygdala: Key to pathological states? Ann. N. Y. Acad. Sci. 2003, 985, 263–272. [CrossRef] [PubMed]
- Sabri, M.; Radnovich, A.J.; Li, T.Q.; Kareken, D.A. Neural correlates of olfactory change detection. Neuroimage 2005, 25, 969–974. [CrossRef] [PubMed]
- Plailly, J.; Howard, J.D.; Gitelman, D.R.; Gottfried, J.A. Attention to odor modulates thalamocortical connectivity in the human brain. J. Neurosci. 2008, 28, 5257–5267. [CrossRef] [PubMed]
- Tham, W.W.; Stevenson, R.J.; Miller, L.A. The functional role of the medio dorsal thalamic nucleus in olfaction. Brain Res. Rev. 2009, 62, 109–126. [CrossRef] [PubMed]
- Fredrickson, B.L.; Joiner, T. Positive emotions trigger upward spirals toward emotional wellbeing. Psychol. Sci. 2002, 13, 172–175. [CrossRef] [PubMed]
- Piefke, M.; Weiss, P.H.; Zilles, K.; Markowitsch, H.J.; Fink, G.R. Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. Brain 2003, 126, 650–668. [CrossRef] [PubMed]
- Reid, C.A.; Green, J.D.; Wildschut, T.; Sedikides, C. Scent-evoked nostalgia. Memory 2015, 23, 157–166. [CrossRef] [PubMed]
- Toffolo, M.B.; Smeets, M.A.; van den Hout, M.A. Proust revisited: Odours as triggers of aversive memories. Cognit. Emot. 2012, 26, 83–92. [CrossRef] [PubMed]
- Vermetten, E.; Bremner, J.D. Olfaction as a traumatic reminder in posttraumatic stress disorder: Case reports and review. J. Clin. Psychiatry 2003, 642, 202–207. [CrossRef]
- Masaoka, Y.; Sugiyama, H.; Katayama, A.; Kashiwagi, M.; Homma, I. Slow breathing and emotions associated with odor-induced autobiographical memories. Chem. Sens. 2012, 37, 379–388. [CrossRef] [PubMed]
- Matsunaga, M.; Isowa, T.; Yamakawa, K.; Kawanishi, Y.; Tsuboi, H.; Kaneko, H.; Ohira, H. Psychological and physiological responses to odor-evoked autobiographic memory. Neuroendocrinol. Lett. 2011, 32, 774–80. [PubMed]
- Matsunaga, M.; Bai, Y.; Yamakawa, K.; Toyama, A.; Kashiwagi, M.; Fukuda, K.; Yamada, J. Brain–immune interaction accompanying odor-evoked autobiographic memory. PLoS ONE 2013, 8, e72523. [CrossRef] [PubMed]
- Sayette, M.A.; Parrott, D.J. Effects of olfactory stimuli on urge reduction in smokers. Exp. Clin. Psychopharmacol. 1999, 7, 151–159. [CrossRef] [PubMed]
- Josephson, B.R.; Singer, J.A.; Salovey, P. Mood regulation and memory: Repairing sad moods with happy memories. Cognit. Emot. 1996, 10, 437–444. [CrossRef]
- Panagioti, M.; Gooding, P.A.; Tarrier, N. An empirical investigation of the effectiveness of the broad-minded affective coping procedure (BMAC) to boost mood among individuals with posttraumatic stress disorder (PTSD). Behav. Res. Ther. 2012, 50, 589–595. [CrossRef] [PubMed]
- Barrett, F.S.; Grimm, K.J.; Robins, R.W.; Wildschut, T.; Sedikides, C.; Janata, P. Music-evoked nostalgia: Affect, memory, and personality. Emotion 2010, 10, 390–403. [CrossRef] [PubMed]
- Royet, J.P.; Zald, D.; Versace, R.; Costes, N.; Lavenne, F.; Koenig, O.; Gervais, R. Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: A positron emission tomography study. J. Neurosci. 2000, 20, 7752–7759. [PubMed]
- Pressman, S.D.; Cohen, S. Does positive affect influence health? Psychol. Bull. 2005, 131, 925–971. [CrossRef] [PubMed]
- Herz, R.S. Odor memory and the special role of associative learning. In Olfactory Cognition: From Perception and Memory to Environmental Odours and Neuroscience; Zucco, G.M., Herz, R.S., Schall, B., Eds.; John Benjamins Publishing Company: Amsterdam, The Netherlands, 2012; pp. 95–114.
- Zucco, G.M. The acquisition of odour preferences via evaluative olfactory conditioning: Historical background and state of the art. In Olfactory Cognition: From Perception and Memory to Environmental Odours and Neuroscience; Zucco, G.M., Herz, R.S., Schaal, B., Eds.; John Benjamins Publishing Company: Amsterdam, The Netherlands, 2012; pp. 269–294.
- Engen, T. The acquisition of odor hedonics. In Perfumery: The Psychology and Biology of Fragrance; van Toller, S., Dodd, G.H., Eds.; Chapman & Hall: New York, NY, USA, 1988.
- Herz, R.S. Aromatherapy facts and fictions: A scientific analysis of olfactory effects on mood, physiology and behavior. Int. J. Neurosci. 2009, 119, 263–290. [CrossRef] [PubMed]
- Herz, R. The Scent of Desire: Discovering Our Enigmatic Sense of Smell; William Morrow/HarperCollins Publishers: New York, NY, USA, 2007.
- Fontanini, A.; Bower, J.M. Slow-waves in the olfactory system: An olfactory perspective on cortical rhythms. Trends Neurosci. 2006, 29, 429–437. [CrossRef] [PubMed]
- Bremner, J.D.; Narayan, M. The effects of stress on memory and the hippocampus throughout the life cycle: Implications for childhood development and aging. Dev. Psychopathol. 1998, 10, 871–885. [CrossRef] [PubMed]
- Cohen, S.; Janicki-Deverts, D.; Miller, G.E. Psychological stress and disease. JAMA 2007, 298, 1685–1687. [CrossRef] [PubMed]
- Hammen, C. Stress and depression. Ann. Rev. Clin. Psychol. 2005, 1, 293–319. [CrossRef] [PubMed]
- McBurney, D.H.; Shoup, M.L.; Streeter, S.A. Olfactory comfort: Smelling a partner's clothing during periods of separation. J. Appl. Soc. Psychol. 2006, 36, 2325–2335. [CrossRef]
- Shoup, M.L.; Streeter, S.A.; McBurney, D.H. Olfactory comfort and attachment within relationships. J. Appl. Soc. Psychol. 2008, 38, 2954–2963. [CrossRef]
- Herz, R. Food Sense: A Sensory and Psychological Guide to Eating; W.W. Norton and Co.: New York, NY, USA, 2017; in press.
- Buckland, N.J.; Finlayson, G.; Hetherington, M.M. Pre-exposure to diet-congruent food reduces energy intake in restrained dieting women. Eat. Behav. 2013, 14, 249–254. [CrossRef] [PubMed]
- Kemps, E.; Tiggemann, M. Olfactory stimulation curbs food cravings. Addict. Behav. 2013, 38, 1550–1554. [CrossRef] [PubMed]
- Ohira, H.; Isowa, T.; Nomura, M.; Ichikawa, N.; Kimura, K.; Miyakoshi, M.; Yamada, J. Imaging brain and immune association accompanying cognitive appraisal of an acute stressor. Neuroimage 2008, 39, 500–514. [CrossRef] [PubMed]
- Ohira, H.; Fukuyama, S.; Kimura, K.; Nomura, M.; Isowa, T.; Ichikawa, N.; Yamada, J. Regulation of natural killer cell redistribution by prefrontal cortex during stochastic learning. Neuroimage 2009, 47, 897–907. [CrossRef] [PubMed]
- Maes, M.; Kubera, M.; Obuchowiczwa, E.; Goehler, L.; Brzeszcz, J. Depression’s multiple comorbidities explained by (neuro) inflammatory and oxidative & nitrosative stress pathways. Neuroendocrinol. Lett. 2011, 32, 7–24. [PubMed]
- Yamakawa, K.; Matsunaga, M.; Isowa, T.; Kimura, K.; Kasugai, K.; Yoneda, M.; Ohira, H. Transient responses of inflammatory cytokines in acute stress. Biol. Psychol. 2009, 82, 25–32. [CrossRef] [PubMed]
- Matsunaga, M.; Isowa, T.; Yamakawa, K.; Tsuboi, H.; Kawanishi, Y.; Kaneko, H.; Ohira, H. Association between perceived happiness levels and peripheral circulating pro-inflammatory cytokine levels in middle-aged adults in Japan. Neuroendocrinol. Lett. 2011, 32, 458–463. [PubMed]
- Libby, P. Inflammatory mechanisms: The molecular basis of inflammation and disease. Nutr. Rev. 2007, 65, 140–146. [CrossRef]
- Dalton, P.; Wysocki, C.J. The nature and duration of adaptation following long-term odor exposure. Percept. Psychophys. 1996, 58, 781–792. [CrossRef] [PubMed]
- Stuck, B.A.; Fadel, V.; Hummel, T.; Sommer, J.U. Subjective olfactory desensitization and recovery in humans. Chem. Sens. 2014, 39, 151–157. [CrossRef] [PubMed]
- Czerniawska, E.; Zegardło, E.; Wojciechowski, J. Memories evoked by odors stimulating the olfactory nerve versus odors stimulating both the olfactory and trigeminal nerves: Possible qualitative differences? Percept. Mot. Skills 2013, 117, 248–256. [CrossRef]
- Lawless, H.; Engen, T. Associations to odors: Interference, mnemonics, and verbal labeling. J. Exp. Psychol. Hum. Learn. Mem. 1977, 3, 52–59. [CrossRef]
- Yeshurun, Y.; Lapid, H.; Dudai, Y.; Sobel, N. The privileged brain representation of first olfactory associations. Curr. Biol. 2009, 19, 1869–1874. [CrossRef] [PubMed]
- Lehrner, J.; Marwinski, G.; Lehr, S.; Johren, P.; Deecke, L. Ambient odors of orange and lavender reduce anxiety and improve mood in a dental office. Physiol. Behav. 2005, 86, 92–95. [CrossRef] [PubMed]
- Motomura, N.; Sakurai, A.; Yotsuya, Y. Reduction of mental stress with lavender odorant. Percept. Mot. Skills 2001, 93, 713–718. [CrossRef] [PubMed]
- Campenni, C.E.; Crawley, E.J.; Meier, M.E. Role of suggestion in odor-induced mood change. Psychol. Rep. 2004, 94, 1127–1136. [CrossRef] [PubMed]
- Carskadon, M.A.; Saletin, J.M.; Van Reen, E.; Bartz, A.; Hart, C.; Raynor, H.; Herz, R.S. Circadian influences on smell and taste detection thresholds: Preliminary results from adolescents. Sleep 2015, 38, 213–228.
- Ayabe-Kanamura, S.; Schicker, I.; Laska, M.; Hudson, R.; Distel, H.; Kobayakawa, T.; Saito, S. Differences in perception of everyday odors: A Japanese-German cross-cultural study. Chem. Sens. 1998, 23, 31–38. [CrossRef]
- Keller, A.; Zhuang, H.; Chi, Q.; Vosshall, L.B.; Matsunami, H. Genetic variation in a human odorant receptor alters odour perception. Nature 2007, 449, 468–472. [CrossRef] [PubMed]
- McRae, J.F.; Jaeger, S.R.; Bava, C.M.; Beresford, M.K.; Hunter, D.; Jia, Y.; Chheang, S.L. Identification of regions associated with variation in sensitivity to food-related odors in the human genome. Curr. Biol. 2013, 23, 1596–1600. [CrossRef] [PubMed]
- Menashe, I.; Man, O.; Lancet, D.; Gilad, Y. Different noses for different people. Nat. Genet. 2003, 34, 143–144. [CrossRef] [PubMed]
- Kurz, J. Getting to the Root of the Great Cilantro Divide. Available online: http://www.npr.org/templates/story/story.php?storyId=98695984 (accessed on 26 December 2008).
- Herz, R.S. Olfaction. In Sensation & Perception; Wolfe, J.E., Kluender, K.R., Levi, D.M., Bartoshuk, L.M., Herz, R.S., Klatzky, R.L., Lederman, S.J., Merfeld, D.M., Eds.; Sinauer Associates, Inc.: Sunderland, MA, USA, 2014.
- Doty, R.L.; Cameron, E.L. Sex differences and reproductive hormone influences on human odor perception. Physiol. Beha. 2009, 97, 213–228. [CrossRef] [PubMed]
- Chen, D.; Dalton, P. The effect of emotion and personality on olfactory perception. Chem. Sens. 2005, 30, 345–351. [CrossRef] [PubMed]
- Bell, I.R.; Miller, C.S.; Schwartz, G.E. An olfactory-limbic model of multiple chemical sensitivity syndrome: Possible relationships to kindling and affective spectrum disorders. Biol. Psychiatry 1992, 32, 218–242. [CrossRef]
- Dalton, P. Cognitive influences on health symptoms from acute chemical exposure. Health Psychology 1999, 18, 579–590. [CrossRef] [PubMed]
- Kirk-Smith, M.D.; Van Toller, C.; Dodd, G.H. Unconscious odour conditioning in human subjects. Biol. Psychol. 1983, 17, 221–231. [CrossRef]
- Lehrner, J.; Eckersberger, C.; Walla, P.; Potsch, G.; Deecke, L. Ambient odor of orange in a dental office reduces anxiety and improves mood in female patients. Physiol. Beha. 2000, 71, 83–86. [CrossRef]
- Herz, R.S.; Cupchik, G.C. An experimental characterization of odor-evoked memories in humans. Chem. Sens. 1992, 17, 519–528. [CrossRef]
- Laird, D.A. What can you do with your nose? Sci. Mon. 1935, 41, 126–130.
- Pause, B.M.; Ferstl, R.; Fehm-Wolfsdorf, G. Personality and olfactory sensitivity. J. Res. Personal. 1998, 32, 510–518. [CrossRef]
- Zucco, G.M.; Aiello, L.; Turuani, L.; Köster, E. Odor-evoked autobiographical memories: Age and gender differences along the life span. Chem. Sens. 2012, 37, 179–189. [CrossRef] [PubMed]
- Devriese, S.; Winters, W.; Stegen, K.; van Diest, I.; Veulemans, H.; Nemery, B.; Eelen, P.; van de Woestijne, K.; van den Bergh, O. Generalization of acquired somatic symptoms in response to odors: A Pavlovian perspective on multiple chemical sensitivity. Psychosom. Med. 2000, 62, 751–759. [CrossRef] [PubMed]
- Lee, M.S.; Choi, J.; Posadzki, P.; Ernst, E. Aromatherapy for health care: An overview of systematic reviews. Maturitas 2012, 71, 257–260. [CrossRef] [PubMed]
- Gaillet, M.; Sulmont-Rossé, C.; Issanchou, S.; Chabanet, C.; Chambaron, S. Impact of a non-attentively perceived odour on subsequent food choices. Appetite 2014, 76, 17–22. [CrossRef] [PubMed]
- Croy, I.; Negoias, S.; Novakova, L.; Landis, B.N.; Hummel, T. Learning about the functions of the olfactory system from people without a sense of smell. PLoS ONE 2012, 7, e33365. [CrossRef] [PubMed]
- Smeets, M.A.; Veldhuizen, M.G.; Galle, S.; Gouweloos, J.; de Haan, A.M.J.; Vernooij, J.; Kroeze, J.H. Sense of smell disorder and health-related quality of life. Rehabil. Psychol. 2009, 54, 404–412. [CrossRef] [PubMed]
|Studies Reporting Predominantly Psychological Effects|
|Arshamanian et al., 2013 ||Familiar odors evocative of an AM were compared with memories elicited by verbal labels for those odors during fMRI scanning. Post-scanning, odors and labels were re-assessed and participants provided subjective evaluations of their memories.||Odors elicited more emotional and positive memories, and more activity in parahippocampal, amygdala and tempopolar regions than labels.|
|Miles and Bernsten (2011) ||12 familiar stimuli presented in verbal, visual and olfactory formats were compared for various qualitative dimensions of memory.||Odor-evoked memories were more positive, and more relevant to one’s life story than memories elicited by verbal or visual cues.|
|Reid et al. (2015) ||12 common scents were evaluated for nostalgic evocation and associated feelings.||Higher levels of odor-evoked nostalgia elicited higher levels of positive affect, self-esteem, self and social connectedness, optimism, and life meaning. Nostalgic scents elicited 3× more positive than negative emotions, and 2× more positive emotions than in a previous study examining music-evoked nostalgia.|
|Toffolo et al. (2012) ||An aversive documentary was paired with an olfactory, visual or auditory cue. One week later memories for the documentary were compared.||The olfactory condition elicited more arousing, detailed and unpleasant memories of the documentary than the auditory condition.|
|Willander and Larsson (2007) ||10 common scents were presented in odor-only, verbal-only, and odor + verbal format as memory cues and various experiential factors were assessed.||Odor-only cues elicited the most positive, emotional, and evocative memories.|
|Vermetten and Bremner (2003) ||Case reports of three individuals suffering from odor-evoked PTSD.||Odors specific to a given individual’s past trauma evoked PTSD flashbacks that were intensely negative, persisted for decades, and did not extinguish with time.|
|Studies Reporting Predominantly Physiological Effects|
|Masaoka et al., 2012 ||A self-selected perfume that evoked an AM for each participant was compared to pleasant/neutral CFs.||Odors that evoked AMs promoted deeper, slower and more relaxed breathing compared to the CFs. More evocative memories and deeper breathing was observed among individuals who scored highest in trait anxiety.|
|Matsunaga et al. (2011) ||A self-selected perfume that evoked an AM for each participant was compared to a pleasant unfamiliar CF. Evoked emotions and associations were evaluated using rating scales. HR, SC, and plasma IL-2 levels in response to the odors were measured.||AM fragrances elicited more positive emotion, increased feelings of comfort and happiness, and decreased anxiety compared to the CF. HR decreased, SC increased, and IL-2 decreased after smelling the AM compared to the cf.|
|Matsunaga et al. (2013) ||A self-selected fragrance that evoked an AM for each participant was compared to two pleasant generic CFs. Emotions and memories evoked were evaluated. Plasma TNF-α, IFN-γ and IL levels in response to the odors were measured. PET scans of neurological activity during odor exposure were assessed.||6.5 times more feelings of nostalgia was experienced to the AM than CF. TNF-α and IFN-γ were decreased after smelling the AM. mOFC and precuneus/PCC were significantly activated during AMs, and activity in the mOFC and precuneus/PCC were negatively correlated with IFN-γ concentration. No IL changes were observed.|
|Sayette & Parrot (1999) ||Chronic smokers sniffed either a pleasant odor, an unpleasant odor, or a no-odor control when they experienced a cigarette craving.||Sniffing odors reduced cravings for cigarettes compared to the control condition. There was a trend for odors that evoked a memory to be the most effective at diminishing urges.|
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