Skip to main content Accessibility help
  • Cited by 5
  • Print publication year: 2006
  • Online publication date: August 2009

4 - Olfaction and Memory

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


This chapter analyzes the nature of olfactory memory in an attempt to understand its uniqueness and richness. It summarises neurobiological underpinnings of olfactory memory before discussing specific issues pertaining to components of the olfactory memory system. The chapter also presents a discussion of the nature of olfactory memory encoding and retrieval in relation to semantic processes and an assessment of the relationship between emotion and olfactory memories. The memory studies probe explicit memory for odours. However, olfaction plays an important role in the implicit and unconscious component of memory. The olfactory memory system may rely upon cross-modal integration, and incongruent cues could attenuate olfactory memory retrieval. Olfactory perceptual qualities, such as hedonics and familiarity, are autonomic in nature and influence olfactory stimulus encoding. The context in which olfactory stimuli are encoded is likely to influence olfactory memory retrieval.
Abraham, A. & Mathai, K. V. (1983) The effect of right temporal lobe lesions on matching of smells. Neuropsychologia, 21, 277–81.
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.
Arnold, S. E. & Trojanowski, J. Q. (1996) Human fetal hippocampal development: I. Cytoarchitecture, myeloarchitecture, and neuronal morphologic features. J Comp Neurol, 367, 274–92.
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.
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.
Buchanan, T. W., Tranel, D., & Adolphs, R. (2003) A specific role for the human amygdala in olfactory memory. Learn Mem, 10, 319–25.
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.
Bensafi, M., Rouby, C., Farget, V., et al. (2002b) Psychophysiological correlates of affects in human olfaction. Neurophysiol Clin, 32, 326–32.
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.
Cain, W. (1979) To know with the nose: keys to odor identification. Science, 203, 467–70.
Cain, W. S., Schiet, F. T., Olsson, M. J., et al. (1995) Comparison of models of odor interaction. Chem Senses, 20, 625–37.
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.
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.
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.
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.
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.
Chu, S. & Downess, J. J. (2000) Odour-evoked autobiographical memories: psychological investigations of proustian phenomena. Chem Senses, 25, 111–16.
Chu, S., & Downess, J. J. (2002) Proust nose best: odors are better cues of autobiographical memory. Mem Cognit, 30, 511–18.
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.
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.
Dalton, P. (1996) Odor perception and beliefs about risk. Chem Senses, 21, 447–58.
Dalton, P. (2000) Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses, 25, 487–92.
Wijk, R. A. & Cain, W. S. (1994) Odor quality: discrimination versus free and cued identification. Percept Psychophys, 56, 12–18.
Distel, H. & Hudson, R. (2001) Judgement of odor intensity is influenced by subjects' knowledge of the odor source. Chem Senses, 26, 247–51.
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.
Ehrlichman, H., Brown, S., Zhu, J., et al. (1995) Startle reflex modulation during exposure to pleasant and unpleasant odors. Psychophysiology, 32, 150–4.
Eichenbaum, H. (1998) Using olfaction to study memory. Ann N Y Acad Sci, 855, 657–69.
Eichenbaum, H., Clegg, R. A. & Feeley, A. (1983) Reexamination of functional subdivisions of the rodent prefrontal cortex. Exp Neurol, 79, 434–51.
Engen, T. (1983) The human uses of olfaction. Am J Otolaryngol, 4, 250–1.
Engen, T. (1987) Remembering odors and their names. Am Scientist, 75, 497–503.
Engen, T. & Ross, B. M. (1973) Long-term memory of odors with and without verbal descriptions. J Exp Psychol, 100, 221–7.
Frey, S. & Petrides, M. (2000) Orbitofrontal cortex: A key prefrontal region for encoding information. Proc Natl Acad Sci USA, 97, 8723–7.
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.
Fuster, J. M. (1997) Network memory. Trends Neurosci, 20, 451–9.
Goldman-Rakic, P. S. (1995) Architecture of the prefrontal cortex and the central executive. Ann NY Acad Sci, 769, 71–83.
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.
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.
Herz, R. S. & Cupchik, G. C. (1995) The emotional distinctiveness of odor-evoked memories. Chem Senses, 20, 517–28.
Herz, R. S., Eliassen, J., Beland, S., et al. (2004) Neuroimaging evidence for the emotional potency of odor-evoked memory. Neuropsychologia, 42, 371–8.
Holmes, D. D. (1970) Differential changes in affective intensity and forgetting of unpleasant personal experiences. J Personality Soc Psychol, 15, 234.
Hummel, T. & Kobal, G. (1992) Differences in human evoked potentials related to olfactory or trigeminal chemosensory activation. Electroencephalogr Clin Neurophysiol, 84, 84–9.
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.
Jones-Gotman, M. & Zatorre, R. J. (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia, 26, 387–400.
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.
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.
Lehrner, J. P., Walla, P., Laska, M., et al. (1999) Different forms of human odor memory: a developmental study. Neurosci Letters, 272, 17–20.
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.
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.
Lipton, P. A., Alvarez, P. & Eichenbaum, H. (1999) Crossmodal associative memory representations in rodent orbitofrontal cortex. Neuron, 22, 349–59.
Lorig, T. S. (1999) On the similarity of odor and language perception. Neurosci Biobehav Rev, 23, 391–8.
Lorig, T. S., Elmes, D. G. & Yoerg, V. L. (1998) Chemosensory alteration of information processing. Ann NY Acad Sci, 855, 591–7.
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.
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.
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.
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.
Mouly, A. M. & Gervais, R. (2002) Polysynaptic potentiation at different levels of rat olfactory pathways following learning. Learn Mem, 9, 66–75.
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.
Murphy, C. & Cain, W. S. (1986) Odor identification: the blind are better. Physiol Behav, 37, 177–180.
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.
Olsson, M. J. (1999) Implicit testing of odor memory: instances of positive and negative repetition priming. Chem Senses, 24, 347–50.
Olsson, M. J. & Cain, W. S. (2003) Implicit and explicit memory for odors: hemispheric differences. Mem Cognit, 31, 44–50.
Olsson, M. J. & Friden, M. (2001) Evidence of odor priming: edibility judgements are primed differently between the hemispheres. Chem Senses, 26, 117–23.
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.
Petrides, M. (1995) Functional organization of the human frontal cortex for mnemonic processing. Evidence from neuroimaging studies. Ann NY Acad Sci, 769, 85–96.
Powell, T. P., Cowan, W. M. & Raisman, G. (1965) The central olfactory connexions. J Anat, 99, 791–813.
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.
Rausch, R., Serafetinides, E. A. & Crandall, P. H. (1977) Olfactory memory in patients with anterior temporal lobectomy. Cortex, 13, 445–52.
Rolls, E. T. (2000) Memory systems in the brain. Ann Rev Psychol, 51, 599–630.
Rolls, E. T. & Baylis, L. L. (1994) Gustatory, olfactory and visual convergence within the primate orbitofrontal cortex. J Neuroscience, 14, 5437–52.
Rolls, E. T., Critchley, H. D. & Treves, A. (1996) Representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol, 75, 1982–96.
Rosenbluth, R., Grossman, E. S. & Kaitz, M. (2000) Performance of early-blind and sighted children on olfactory tasks. Perception, 29, 101–10.
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.
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.
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.
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.
Rubin, D. C., Groth, E. & Goldsmith, D. J. (1984) Olfactory cuing of autobiographical memory. Am J Psychol, 97, 493–507.
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.
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.
Savic, I. (2001) Processing of odorous signals in humans. Brain Res Bull, 54, 307–12.
Savic, I. & Berglund, H. (2004) Passive perception of odors and semantic circuits. Hum Brain Mapp, 21, 271–8.
Savic, I., Gulyas, B., Larsson, M., et al. (2000) Olfactory functions are mediated by parallel and hierarchical processing. Neuron, 26, 735–45.
Schoenbaum, G., Chiba, A. A. & Gallagher, M. (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci, 1, 155–9.
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.
Tremblay, L. & Schultz, W. (1999) Relative reward preference in primate orbitofrontal cortex. Nature, 398, 704–8.
Tulving, E. & Schacter, D. L. (1990) Priming and human memory systems. Science, 247, 301–6.
Vasterling, J. J., Brailey, K. & Sutker, P. B. (2000) Olfactory identification in combat-related posttraumatic stress disorder. J Trauma Stress, 13, 241–53.
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.
Wakefield, C. E., Homewood, J. & Taylor, A. J. (2004) Cognitive compensations for blindness in children: an investigation using odour naming. Perception, 33, 429–42.
Walla, P., Hufnagl, B., Lehrner, J., et al. (2003) Olfaction and depth of word processing: a magnetoencephalographic study. Neuroimage, 18, 104–16.
Watanabe, M. (1996) Reward expectancy in primate prefrontal neurons. Nature, 382, 629–32.
Watanabe, M. (1998) Cognitive and motivational operations in primate prefrontal neurons. Rev Neurosci, 9, 225–41.
White, I. M. & Wise, S. P. (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res, 126, 315–35.
White, T. L. (1998) Olfactory memory: The long and short of it. Chem Senses, 23, 433–41.
Yamamoto, T., Oomura, Y., Nishino, H., et al. (1984) Monkey orbitofrontal neuron activity during emotional and feeding behaviorsBrain Res Bull, 12, 441–3.
Zajonc, R. B. (1968) Attitudinal effects of mere exposure. J Personality Soc Psy, 9, 1.
Zald, D. H. & Pardo, J. (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol, 36, 165–81.
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.
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.
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.
Zatorre, R. & Jones-Gotman, M. (1991) Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain, 114, 71–84.
Zatorre, R., Jones-Gotman, M. & Rouby, C. (2000) Neural mechanisms involved in odor pleasantness and intensity judgements. Neuroreport, 11, 2711–16.
Zellner, D. A. & Kautz, M. A. (1990) Color affects perceived odor intensity. J Exp Psychol Hum PerceptPerform, 16, 391–7.