Olfaction and Memory

doi:10.1017/CBO9780511543623.006

4 - Olfaction and Memory

from Section I - Neurology, Neurophysiology and Neuropsychology: Olfactory Clues to Brain Development and Disorder

Published online by Cambridge University Press: 17 August 2009

Warrick Brewer and

Edited by

David Castle and

Foreword by

Warrick J. Brewer: Affiliation:
Mental Health Research Institute of Victoria, Melbourne
David Castle: Affiliation:
University of Melbourne
Christos Pantelis: Affiliation:
University of Melbourne

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Summary

The scent was so heavenly fine that tears welled into Baldini's eyes. He did not have to test it; he simply stood at the table in front of the mixing bottle and breathed. The perfume was glorious. It was to Amour and Psyche as a symphony is to the scratching of a lonely violin. And it was more. Baldini closed his eyes and watched as the most sublime memories were awakened within him. He saw himself as a young man walking through the evening gardens of Naples; he saw himself lying in the arms of a woman with dark curly hair and saw the silhouette of a bouquet of roses on the windowsill as the night wind passed by; he heard the random song of birds and the distant music from a harbor tavern; he heard whispering at his ear, he heard I-love-you and felt his hair ruffle with bliss, now! Now at this very moment! He forced open his eyes and groaned with pleasure. This perfume was not like any perfume known before. It was not a scent that made things smell better, not some sachet, some toiletry. It was something completely new, capable of creating a whole world, a magical rich world, and in an instant you forgot all the loathsomeness around you and felt so rich, so at ease, so free, so fine …

-from Perfume by Patrick Süskind

Introduction

As Süskind has reminded us in his evocative description of the power of scent, the slightest hint of perfume can transform the present into the past; it can re-create entire sensory experiences by providing an emotional link between past events initially experienced through separate senses; it can make memories seem real and tangible.

Keywords

cross-modal integration olfactory memory olfactory memory retrieval olfactory stimulus encoding semantic processes

Type: Chapter
Information: Olfaction and the Brain , pp. 65 - 82

DOI: https://doi.org/10.1017/CBO9780511543623.006 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2006

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References

Abraham, A. & Mathai, K. V. (1983) The effect of right temporal lobe lesions on matching of smells. Neuropsychologia, 21, 277–81.Google Scholar

Alaoui-Ismaili, O., Vernet-Maury, E., Dittmar, A., et al. (1997) Odor hedonics: connection with emotional response estimated by autonomic parameters. Chem Senses, 22, 237–48.Google Scholar

Arnold, S. E. & Trojanowski, J. Q. (1996) Human fetal hippocampal development: I. Cytoarchitecture, myeloarchitecture, and neuronal morphologic features. J Comp Neurol, 367, 274–92.Google Scholar

Ayabe-Kanamura, S., Saito, S., Distel, H., et al. (1998) Differences and similarities in the perception of everyday odors. A Japanese-German cross-cultural study, Ann N Y Acad Sci, 855, 694–700.Google Scholar

Baylis, L. L., Rolls, E. T. & Baylis, G. C. (1995) Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate. Neuroscience, 64, 801–12.Google Scholar

Buchanan, T. W., Tranel, D., & Adolphs, R. (2003) A specific role for the human amygdala in olfactory memory. Learn Mem, 10, 319–25.Google Scholar

Bensafi, M., Rouby, C., Farget, V., et al. (2002a) Autonomic nervous system responses to odours: the role of pleasantness and arousal. Chem Senses, 27, 703–9.Google Scholar

Bensafi, M., Rouby, C., Farget, V., et al. (2002b) Psychophysiological correlates of affects in human olfaction. Neurophysiol Clin, 32, 326–32.Google Scholar

Buchanan, T. W., Denburg, N. L., Tranel, D., et al. (2001) Verbal and nonverbal emotional memory following unilateral amygdala damage. Learn Mem, 8, 326–35.Google Scholar

Cain, W. (1979) To know with the nose: keys to odor identification. Science, 203, 467–70.Google Scholar

Cain, W. S., Schiet, F. T., Olsson, M. J., et al. (1995) Comparison of models of odor interaction. Chem Senses, 20, 625–37.Google Scholar

Carmichael, S. T. & Price, J. L. (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol, 346, 366–402.Google Scholar

Carmichael, S. T. & Price, J. L. (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol, 363, 642–64.Google Scholar

Carmichael, S. T. & Price, J. L. (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol, 371, 179–207.Google Scholar

Cavada, C., Company, T., Tejedor, J., et al. (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex, 10, 220–42.Google Scholar

Chiavaras, M. M., LeGoualher, G., Evans, A., et al. (2001) Three-dimensional probabilistic atlas of the human orbitofrontal sulci in standardized stereotaxic space. Neuroimage, 13, 479–96.Google Scholar

Chu, S. & Downess, J. J. (2000) Odour-evoked autobiographical memories: psychological investigations of proustian phenomena. Chem Senses, 25, 111–16.Google Scholar

Chu, S., & Downess, J. J. (2002) Proust nose best: odors are better cues of autobiographical memory. Mem Cognit, 30, 511–18.Google Scholar

Dade, L. A., Zatorre, R. J., Evans, A. C., et al. (2001) Working memory in another dimension: functional imaging of human olfactory working memory. Neuroimage, 14, 650–60.Google Scholar

Dade, L. A., Zatorre, R. J. & Jones-Gotman, M. (2002) Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain, 125, 86–101.Google Scholar

Dalton, P. (1996) Odor perception and beliefs about risk. Chem Senses, 21, 447–58.Google Scholar

Dalton, P. (2000) Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses, 25, 487–92.Google Scholar

Wijk, R. A. & Cain, W. S. (1994) Odor quality: discrimination versus free and cued identification. Percept Psychophys, 56, 12–18.Google Scholar

Distel, H. & Hudson, R. (2001) Judgement of odor intensity is influenced by subjects' knowledge of the odor source. Chem Senses, 26, 247–51.Google Scholar

Distel, H., Ayabe-Kanamura, S., Martinez-Gomez, M., et al. (1999) Perception of everyday odors: correlation between intensity, familiarity and strength of hedonic judgement. Chem Senses, 24, 191–9.Google Scholar

Ehrlichman, H., Brown, S., Zhu, J., et al. (1995) Startle reflex modulation during exposure to pleasant and unpleasant odors. Psychophysiology, 32, 150–4.Google Scholar

Eichenbaum, H. (1998) Using olfaction to study memory. Ann N Y Acad Sci, 855, 657–69.Google Scholar

Eichenbaum, H., Clegg, R. A. & Feeley, A. (1983) Reexamination of functional subdivisions of the rodent prefrontal cortex. Exp Neurol, 79, 434–51.Google Scholar

Engen, T. (1983) The human uses of olfaction. Am J Otolaryngol, 4, 250–1.Google Scholar

Engen, T. (1987) Remembering odors and their names. Am Scientist, 75, 497–503.Google Scholar

Engen, T. & Ross, B. M. (1973) Long-term memory of odors with and without verbal descriptions. J Exp Psychol, 100, 221–7.Google Scholar

Frey, S. & Petrides, M. (2000) Orbitofrontal cortex: A key prefrontal region for encoding information. Proc Natl Acad Sci USA, 97, 8723–7.Google Scholar

Fulbright, R. K., Skudlarski, P., Lacadie, C. M., et al. (1998) Functional MR imaging of regional brain responses to pleasant and unpleasant odors. Am J Neuroradiol, 19, 1721–6.Google Scholar

Fuster, J. M. (1997) Network memory. Trends Neurosci, 20, 451–9.Google Scholar

Goldman-Rakic, P. S. (1995) Architecture of the prefrontal cortex and the central executive. Ann NY Acad Sci, 769, 71–83.Google Scholar

Gottfried, J. A. & Dolan, R. J. (2003) The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron, 39, 375–86.Google Scholar

Gottfried, J. A., Smith, A. P., Rugg, M. D., et al. (2004) Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron, 42, 687–95.Google Scholar

Herz, R. S. & Cupchik, G. C. (1995) The emotional distinctiveness of odor-evoked memories. Chem Senses, 20, 517–28.Google Scholar

Herz, R. S., Eliassen, J., Beland, S., et al. (2004) Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia, 42, 371–8.Google Scholar

Holmes, D. D. (1970) Differential changes in affective intensity and forgetting of unpleasant personal experiences. J Personality Soc Psychol, 15, 234.Google Scholar

Hummel, T. & Kobal, G. (1992) Differences in human evoked potentials related to olfactory or trigeminal chemosensory activation. Electroencephalogr Clin Neurophysiol, 84, 84–9.Google Scholar

Jinks, A., Laing, D. G., Hutchinson, I., et al. (1998) Temporal processing of odor mixtures reveals that identification of components takes precedence over temporal information in olfactory memory. Ann NY Acad Sci, 855, 834–6.Google Scholar

Jones-Gotman, M. & Zatorre, R. J. (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia, 26, 387–400.Google Scholar

Koenig, O., Bourron, G. & Royet, J. P. (2000) Evidence for separate perceptive and semantic memories for odours: a priming experiment. Chem Senses, 25, 703–8.Google Scholar

Kosslyn, S. M., Chabris, C. F., Marsolek, C. J., et al. (1992) Categorical versus coordinate spatial relations: computational analyses and computer simulations. J Exp Psychol Hum Percept Perform, 18, 562–77.Google Scholar

Lehrner, J. P., Walla, P., Laska, M., et al. (1999) Different forms of human odor memory: a developmental study. Neurosci Letters, 272, 17–20.Google Scholar

Levy, L. M., Henkin, R. I., Lin, C. S., et al. (1999) Odor memory induces brain activation as measured by functional MRI. J Comp Assisted Tom, 23, 487–98.Google Scholar

Levy, D. A., Manns, J. R., Hopkins, R. O., et al. (2003) Impaired visual and odor recognition memory span in patients with hippocampal lesions. Learn Mem, 10, 531–6.Google Scholar

Lipton, P. A., Alvarez, P. & Eichenbaum, H. (1999) Crossmodal associative memory representations in rodent orbitofrontal cortex. Neuron, 22, 349–59.Google Scholar

Lorig, T. S. (1999) On the similarity of odor and language perception. Neurosci Biobehav Rev, 23, 391–8.Google Scholar

Lorig, T. S., Elmes, D. G. & Yoerg, V. L. (1998) Chemosensory alteration of information processing. Ann NY Acad Sci, 855, 591–7.Google Scholar

Maylor, E. A., Carter, S. M. & Hallett, E. L. (2002) Preserved olfactory cuing of autobiographical memories in old age. J Gerontol B Psychol Sci Soc Sci, 57, 41–6.Google Scholar

McNamara, T. P., Halpin, J. A. & Hardy, J. K. (1992) The representation and integration in memory of spatial and nonspatial information. Mem Cognit, 20, 519–32.Google Scholar

Melcher, J. M. & Schooler, J. W. (1996) The misremembrance of wines past: Verbal and perceptual expertise differentially mediate verbal overshadowing of taste memory. J Mem Language, 35, 231–45.Google Scholar

Mohr, C., Röhrenbach, C. M., Landis, T., et al. (2001) Associations to smell are more pleasant than to sound. J Clin Exp Neuropsychology, 23, 484–9.Google Scholar

Mouly, A. M. & Gervais, R. (2002) Polysynaptic potentiation at different levels of rat olfactory pathways following learning. Learn Mem, 9, 66–75.Google Scholar

Mouly, A. M., Fort, A., Ben-Boutayab, N., et al. (2001) Olfactory learning induces differential long-lasting changes in rat central olfactory pathways. Neuroscience, 102, 11–21.Google Scholar

Murphy, C. & Cain, W. S. (1986) Odor identification: the blind are better. Physiol Behav, 37, 177–180.Google Scholar

O'Doherty, J. P., Deichmann, R., Critchley, H. D., et al. (2002) Neural responses during anticipation of a primary taste reward. Neuron, 33, 815–26.Google Scholar

Olsson, M. J. (1999) Implicit testing of odor memory: instances of positive and negative repetition priming. Chem Senses, 24, 347–50.Google Scholar

Olsson, M. J. & Cain, W. S. (2003) Implicit and explicit memory for odors: hemispheric differences. Mem Cognit, 31, 44–50.Google Scholar

Olsson, M. J. & Friden, M. (2001) Evidence of odor priming: edibility judgements are primed differently between the hemispheres. Chem Senses, 26, 117–23.Google Scholar

Parr, W. V., Heatherbell, D. & White, K. G. (2002) Demystifying wine expertise: olfactory threshold, perceptual skill and semantic memory in expert and novice wine judges. Chem Senses, 27, 747–55.Google Scholar

Petrides, M. (1995) Functional organization of the human frontal cortex for mnemonic processing. Evidence from neuroimaging studies. Ann NY Acad Sci, 769, 85–96.Google Scholar

Powell, T. P., Cowan, W. M. & Raisman, G. (1965) The central olfactory connexions. J Anat, 99, 791–813.Google Scholar

Price, J. L., Carmichael, S. T. & Drevets, W. C. (1996) Networks related to the orbital and medial prefrontal cortex: a substrate for emotional behavior?Prog Brain Res, 107, 523–36.Google Scholar

Rausch, R., Serafetinides, E. A. & Crandall, P. H. (1977) Olfactory memory in patients with anterior temporal lobectomy. Cortex, 13, 445–52.Google Scholar

Rolls, E. T. (2000) Memory systems in the brain. Ann Rev Psychol, 51, 599–630.Google Scholar

Rolls, E. T. & Baylis, L. L. (1994) Gustatory, olfactory and visual convergence within the primate orbitofrontal cortex. J Neuroscience, 14, 5437–52.Google Scholar

Rolls, E. T., Critchley, H. D. & Treves, A. (1996) Representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol, 75, 1982–96.Google Scholar

Rosenbluth, R., Grossman, E. S. & Kaitz, M. (2000) Performance of early-blind and sighted children on olfactory tasks. Perception, 29, 101–10.Google Scholar

Rosenkilde, C. E., Bauer, R. H. & Fuster, J. M. (1981) Single cell activity in ventral prefrontal cortex of behaving monkeys. Brain Res, 209, 375–94.Google Scholar

Royet, J. P., Paugam-Moisy, H., Rouby, C., et al. (1996) Is short-term odour recognition predictable from odour profile?Chem Senses, 21, 553–66.Google Scholar

Royet, J. P., Koenig, O., Gregoire, M. C., et al. (1999) Functional anatomy of perceptual and semantic processing for odors. J Cog Neurosci, 11, 94–109.Google Scholar

Royet, J. P., Zald, D. H., Versace, R., et al. (2000) Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. J Neuroscience, 15, 7752–9.Google Scholar

Rubin, D. C., Groth, E. & Goldsmith, D. J. (1984) Olfactory cuing of autobiographical memory. Am J Psychol, 97, 493–507.Google Scholar

Sanides, F. & Hoffmann, J. (1969) Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. J Hirnforsch, 11, 79–104.Google Scholar

Savage, R., Combs, D. R., Pinkston, J. B., et al. (2002) The role of temporal lobe and orbitofrontal cortices in olfactory memory function. Arch Clin Neuropsychology, 17, 305–18.Google Scholar

Savic, I. (2001) Processing of odorous signals in humans. Brain Res Bull, 54, 307–12.Google Scholar

Savic, I. & Berglund, H. (2004) Passive perception of odors and semantic circuits. Hum Brain Mapp, 21, 271–8.Google Scholar

Savic, I., Gulyas, B., Larsson, M., et al. (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron, 26, 735–45.Google Scholar

Schoenbaum, G., Chiba, A. A. & Gallagher, M. (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci, 1, 155–9.Google Scholar

Süskind, P. (1976) Perfume. Penguin: London.

Thorpe, S. J., Rolls, E. T. & Maddison, S. (1983) The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res, 49, 93–115.Google Scholar

Tremblay, L. & Schultz, W. (1999) Relative reward preference in primate orbitofrontal cortex. Nature, 398, 704–8.Google Scholar

Tulving, E. & Schacter, D. L. (1990) Priming and human memory systems. Science, 247, 301–6.Google Scholar

Vasterling, J. J., Brailey, K. & Sutker, P. B. (2000) Olfactory identification in combat-related posttraumatic stress disorder. J Trauma Stress, 13, 241–53.Google Scholar

Vermetten, E. & Bremner, J. D. (2003) Olfaction as a traumatic reminder in posttraumatic stress disorder: case reports and review. J Clin Psychiatry, 64, 202–7.Google Scholar

Wakefield, C. E., Homewood, J. & Taylor, A. J. (2004) Cognitive compensations for blindness in children: an investigation using odour naming. Perception, 33, 429–42.Google Scholar

Walla, P., Hufnagl, B., Lehrner, J., et al. (2003) Olfaction and depth of word processing: a magnetoencephalographic study. Neuroimage, 18, 104–16.Google Scholar

Watanabe, M. (1996) Reward expectancy in primate prefrontal neurons. Nature, 382, 629–32.Google Scholar

Watanabe, M. (1998) Cognitive and motivational operations in primate prefrontal neurons. Rev Neurosci, 9, 225–41.Google Scholar

White, I. M. & Wise, S. P. (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res, 126, 315–35.Google Scholar

White, T. L. (1998) Olfactory memory: The long and short of it. Chem Senses, 23, 433–41.Google Scholar

Yamamoto, T., Oomura, Y., Nishino, H., et al. (1984) Monkey orbitofrontal neuron activity during emotional and feeding behaviorsBrain Res Bull, 12, 441–3.Google Scholar

Zajonc, R. B. (1968) Attitudinal effects of mere exposure. J Personality Soc Psy, 9, 1.Google Scholar

Zald, D. H. & Pardo, J. (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol, 36, 165–81.Google Scholar

Zald, D. H. & Pardo, J. V. (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA, 94, 4119–24.Google Scholar

Zald, D. H. & Kim, S. W. (1996a) Anatomy and function of the orbital frontal cortex. II. Function and relevance to obsessive-compulsive disorder. J Neuropsychiatry, 8, 249–61.Google Scholar

Zald, D. H. & Kim, S. W. (1996b) Anatomy and function of the orbital frontal cortex, I: anatomy, neurocircuitry, and obsessive-compulsive disorder. J Neuropsychiatry Clin Neurosci, 8, 125–38.Google Scholar

Zatorre, R. & Jones-Gotman, M. (1991) Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain, 114, 71–84.Google Scholar

Zatorre, R., Jones-Gotman, M. & Rouby, C. (2000) Neural mechanisms involved in odor pleasantness and intensity judgements. Neuroreport, 11, 2711–16.Google Scholar

Zellner, D. A. & Kautz, M. A. (1990) Color affects perceived odor intensity. J Exp Psychol Hum PerceptPerform, 16, 391–7.Google Scholar

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