Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-02T22:28:41.444Z Has data issue: false hasContentIssue false

2 - Olfaction and the Temporal Lobes

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

Published online by Cambridge University Press:  17 August 2009

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

Summary

Introduction

There was a time in the history of anatomy and medicine when the temporal lobes were considered to be the olfactory brain. In an early paper describing a patient with a brain tumor and olfactory auras, Jackson and Beevor (1889a) refer to the ‘anterior tip of the temporo-sphenoidal lobe’ as the ‘pyriform or hippocampal lobule’ (p. 350). They also mention that Broca had described this part of the brain as being well developed in animals with a keen sense of smell, and as being rudimentary in animals with poorer smelling. Since then, our understanding of temporal-lobe function has evolved greatly. We know that the temporal lobes are heterogeneous structures consisting of several subregions, and that this complex set of structures participates in a wide variety of cognitive and emotional functions and behaviors. However, the old wisdom that the temporal lobes have a great importance in olfaction is still valid, and in this chapter, we review the main findings elucidating this relationship.

A brief overview: anatomy and uniqueness of the olfactory system

In most senses, the primary sensory area consists of one region, and adjacent areas usually constitute the secondary sensory regions. In olfaction, however, a whole series of structures constitutes the primary olfactory cortex (POC), and interestingly, some of these structures are not cortical. Carmichael et al. (1994) listed eight principal structures that constitute the POC in the macaque monkey, and a similar composition can be assumed in humans: the anterior olfactory nucleus, the ventral tenia tecta, the piriform cortex, the olfactory tubercle, the periamygdaloid cortex, the nucleus of the lateral olfactory tract of the amygdala, the anterior cortical nucleus of the amygdala and the rostral entorhinal cortex.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, A. & Mathai, K. V. (1983) The effect of right temporal lobe lesions on matching of smells. Neuropsychologia, 21, 277–81.Google Scholar
Acharya, V., Acharya, J. & Lüders, H. (1998) Olfactory epileptic auras. Neurol, 51, 56–61.Google Scholar
Anderson, A. K., Christoff, K., Stappen, I., et al. (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci, 6, 196–202.Google Scholar
Andy, O. J. (1967) The amygdala and hippocampus in olfactory aura, Electroencephalogr Clin Neurophysiol, 23, 291–3.Google Scholar
Andy, O. J., Jurko, M. F. & Hughes, J. R. (1975) The amygdala in relation to olfaction. Confinia Neurologica, 37, 215–22.Google Scholar
Bengtsson, S., Berglund, H., Gulyas, B., et al. (2001) Brain activation during odor perception in males and females. Neuroreport, 12, 2027–33.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., Clugnet, M. C. & Price, J. L. (1994) Central olfactory connections in the Macaque monkey. J Comp Neurol, 346, 413–34.Google Scholar
Carrol, B., Richardson, J. T. E. & Thompson, P. (1993) Olfactory information processing and temporal lobe epilepsy. Brain Cog, 22, 230–43.Google Scholar
Cerf-Ducastel, B. & Murphy, C. (2001) fMRI activation in response to odorants orally delivered in aqueous solutions. Chem Senses, 26, 625–37.Google Scholar
Chen, C., Shih, Y. H., Yen, D. J., et al. (2003) Olfactory auras in patients with temporal lobe epilepsy. Epilepsia, 44, 257–60.Google Scholar
Cleland, T. A. & Linster, C. (2003) Central olfactory structures. In Handbook of Olfaction and Gustation (ed Doty, R. L.), pp. 165–80. New York: Marcel Dekker, Inc.
Dade, L. A., Jones-Gotman, M., Zatorre, R. J., et al. (1998) Human brain function during odor encoding and recognition: A PET activation study. Ann N Y Acad Sci, 855, 572–4.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, 96–101.Google Scholar
Daly, D. (1958) Uncinate fits. Neurol, 8, 250–60.Google Scholar
Djordjevic, J., Zatorre, R. J., Petrides, M., et al. (2004) Functional neuroimaging of odor imagery. Neuroimage, 24, 791–801.
Eichenbaum, H., Morton, T. H., Potter, H., et al. (1983) Selective olfactory deficits in case H.M. Brain, 106, 459–72.Google Scholar
Eskenazi, B., Cain, W. S., Novelly, R. A., et al. (1983) Olfactory functioning in temporal lobectomy. Neuropsychologia, 21, 365–74.Google Scholar
Eskenazi, B.; Cain, W. S.; Novelly, R. A.et al. (1986) Odor perception in temporal lobe epilepsy patients with and without temporal lobectomy. Neuropsychologia, 24, 553–62.Google Scholar
Gastaut, H., Roger, J. & Giove, C. (1955) Troubles de l'olfaction, de la gustation et de l'appétit chez les épileptiques psychomoteurs. Annales de le Med-psychol, 113, 177–206.Google Scholar
Gloor, P., Olivier, A., Quesney, L. F., et al. (1982) The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Annal Neurol, 12, 129–44.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., Deichman, R., Winston, J. S., et al. (2002a) Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci, 22, 10819–28.Google Scholar
Gottfried, J. A., O'Doherty, J. & Dolan, R. J. (2002b) Appetitive and aversive olfactory learning in humans studies using event-related functional magnetic resonance imaging. J Neurosci, 22, 10829–37.Google Scholar
Gottfried, J. A., O'Doherty, J. & Dolan, R. J. (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301, 1104–7.Google Scholar
Gottfried, J. A., Smith, A. P. R., Rugg, M. D., et al. (2004) Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron, 42, 687–95.Google Scholar
Greenberg, M. S. (1992) Olfactory hallucinations. In Science of Olfaction (Serby, M. J. & Chobor, K. L., eds), pp. 467–99. New York: Springer-Verlag.
Gupta, A. K., Jeavons, P. M., Hughes, R. C., et al. (1983) Aura in temporal lobe epilepsy: clinical and electrophysiological correlation. J Neurol Neurosurg Psychiatry, 46, 1079–83.Google Scholar
Haberly, L. B. (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses, 26, 551–76.Google Scholar
Halgren, E., Walter, R. D., Cherlow, D. G., et al. (1978) Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain, 101, 83–117.Google Scholar
Herz, R. S., Eliassen, J., Beland, S., et al. (2004) Neuroimaging evidence for emotional potency of odor-evoked memory. Neuropsychologia, 42, 371–8.Google Scholar
Howe, J. G. & Gibson, J. D. (1982) Uncinate seizures and tumors: a myth re-examined. Ann Neurol, 12, 227.Google Scholar
Hudry, J., Ryvlin, P., Royet, J. P., et al. (2001) Odorants elicit evoked potentials in the human amygdala. Cereb Cortex, 11, 619–27.Google Scholar
Hudry, J., Perrin, F., Ryvlyn, P., et al. (2003) Olfactory short-term memory and related amygdala recordings in patients with temporal lobe epilepsy. Brain, 126, 1851–63.Google Scholar
Hudry, J., Pouliot, S., Gotman, J., et al. (2004) Memory for emotional and neutral odors and amygdala electrophysiological recordings in patients with epilepsy. Chem Senses, 30, 275.Google Scholar
Hummel, T., Livermore, A., Hummel, C., et al. (1992) Chemosensory evoked potentials: relations to olfactory and trigeminal sensations. Electroencephalogra Clin Neurophysiol, 84, 192–5.Google Scholar
Hummel, T., Pauli, E., Schüler, P., et al. (1995) Chemosensory event-related potentials in patients with temporal lobe epilepsy. Epilepsia, 36, 79–85.Google Scholar
Jackson, J. H. (1871) Notes from the out-patient practice of Dr. Hughlings Jackson. Lancet, March 18, 376–7.Google Scholar
Jackson, J. H. & Beevor, C. E. (1889a) Case of tumour of the right temporo-sphenoidal lobe bearing on the localisation of the sense of smell and on the interpretation of a particular variety of epilepsy. Brain, 33, 346–57.Google Scholar
Jackson, J. H. & Beevor, C. E. (1889b) Epilepsy with olfactory aura. Lancet, February 23, 381–2.Google Scholar
Jackson, J. H. & Stewart, P. (1899) Epileptic attacks with a warning of a crude sensation of smell and with the intellectual aura (dreamy state) in a patient who had symptoms pointing to gross organic disease of the right temporo-sphenoidal lobe. Brain, 33, 534–49.Google Scholar
Jasper, H. H. & Rasmussen, T. (1958) Studies of clinical and electrical responses to deep temporal stimulation in man with some considerations of functional anatomy. Res Publ Assoc Res Nerv Ment Dis, 36, 316–34.Google Scholar
Johnson, D. M. G., Illig, K. R., Behan, M., et al. (2000) New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that ‘primary’ olfactory cortex functions like ‘association’ cortex in other sensory systems. J Neurosci, 20, 6974–82.Google Scholar
Jones-Gotman, M. & Zatorre, R. J. (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia, 26, 387–400.Google Scholar
Jones-Gotman, M. & Zatorre, R. J. (1993) Odor recognition memory in humans: Role of right temporal and orbitofrontal regions. Brain Cognition, 22, 182–98.Google Scholar
Jones-Gotman, M., Zatorre, R. J., Evans, A. C., et al. (1993) Functional activation of right hippocampus during an olfactory recognition memory task. Soc Neurosci Ab, 19, 1002.Google Scholar
Jones-Gotman, M., Zatorre, R. J., Cendes, F., et al. (1997) Contribution of medial versus lateral temporal-lobe structures to human odour identification. Brain, 120, 1845–56.Google Scholar
Kareken, D. A., Sabri, M., Radnovich, A. J., et al. (2004) Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex. Neuroimage, 22, 456–65.Google Scholar
Kohler, C. G., Moberg, P. J., Gur, R. E., et al. (2001) Olfactory dysfunction in schizophrenia and temporal lobe epilepsy. Neuropsychiatr Neuropsychology Beh Neurol, 14, 83–8.Google Scholar
Lehrner, J., Baumgatner, C., Serles, W., et al. (1997) Olfactory prodromal symptoms and unilateral olfactory dysfunction are associated in patients with right mesial temporal lobe epilepsy. Epilepsia, 38, 1042–4.Google Scholar
Lennox, W. G. & Cobb, S. (1933) Epilepsy XIII. Aura in Epilepsy: a statistical review of 1,359 cases. Arch Neurol Psychiatry, 30, 374–87.Google Scholar
Levy, L. M., Henkin, R. I., Hutter, A., et al. (1997) Functional MRI of human olfaction. J Comput Assist Tomogr, 21, 849–56.Google Scholar
Mai, J. K., Assheuer, J. & Paxinos, G. (1997) Atlas of the Human Brain. San Diego: Academic Press.
Manford, M. & Shorvon, S. D. (1992) Prolonged sensory or visceral symptoms: an under-diagnosed form of non-convulsive focal (simple partial) status epilepticus. J Neurol Neurosurg Psychiatry, 55, 714–16.Google Scholar
Martinez, B. A., Cain, W. S., Wijk, R. A., et al. (1993) Olfactory functioning before and after temporal lobe resection for intractable seizures. Neuropsychology, 7, 351–63.Google Scholar
Mizobuchi, M., Ito, N., Tanaka, C., et al. (1999) Unidirectional olfactory hallucination associated with ipsilateral unruptured intracranial aneurism. Epilepsia, 40, 516–19.Google Scholar
Nashold, B. S. & Wilson, W. P. (1970) Olfactory hallucinations evoked from stimulation of human thalamus. Confinia Neurologica, 32, 298–307.Google Scholar
Olivier, A. & Boling, W. (2000) Stereotactic intracranial recording (Stereoelectroencephalography). In Operative Neurological Techniques Indications, Methods & Results, (Fourth Ed), Vol 2 (ed Schmidek, H. H.), pp. 1511–28. Philadelphia: W.B. Saunders Company.
Penfield, W. & Jasper, H. (1954) Epilepsy and the Functional Anatomy of the Human Brain. Little, Brown and Company: Boston.
Penfield, W. & Perot, P. (1963) The brain's record of auditory and visual experience. Brain, 86, 595–696.Google Scholar
Petrides, M. & Pandya, D. N. (1994) Comparative architectonic analysis of the human and the Macaque frontal cortex. InHandbook of Neuropsychology, Vol. 9 (eds F. Boller & J. Grafman), pp. 17–58. Amsterdam: Elsevier Science.Google Scholar
Poellinger, A., Thomas, R., Lio, P., et al. (2001) Activation and habituation in olfaction – An fMRI study. Neuroimage, 13, 547–60.Google Scholar
Potolicchio, S. J., Lossong, J. H., O'Dohertt, D. S., et al. (1986) Partial seizures with simple psychosensory symptomatology (cyclic phantosmia): a new and distinct seizure disorder. Clin Res, 34, 635A.Google Scholar
Price, J. L. (1985) Beyond the primary olfactory cortex: olfactory-related areas in the neocortex, thalamus and hypothalamus. Chem Senses, 10, 230–58.Google Scholar
Price, J. L. (1987) The central olfactory and accessory olfactory systems. In Neurobiology of Taste and Smell (eds Finger, T. E. & Silver, W. L.), pp. 179–204. New York: Wiley.
Price, J. L. (1990) Olfactory system. In The Human Nervous System (ed Paxinos, G.), pp. 980–98. San Diego: Academic Press.
Price, J. L., Carmichael, S. T., Carnes, K. M., et al. (1991) Olfactory input to the prefrontal cortex. In Olfaction: A Model System for Computational Neuroscience (eds Davis, J. & Eichenbaum, H.), pp. 101–20. Cambridge, MA: MIT Press.
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., Kringelbach, M. L. & Araujo, I. E. T. (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci, 18, 695–703.Google Scholar
Royet, J. P. & Plailly, J. (2004) Lateralization of olfactory processes. Chem Senses, 29, 731–45.Google Scholar
Royet, J. P., Zald, D., Versace, R., et al. (2000) Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: a positron emission tomography study. J Neurosci, 20, 7752–9.Google Scholar
Royet, J. P., Plailly, J., Delon-Martin, C., et al. (2003) fMRI of emotional responses to odors: influence of hedonic valence and judgment, handedness, and gender. Neuroimage, 20, 713–28.Google Scholar
Savic, I. & Berglund, H. (2004) Passive perception of odors and semantic circuits. Hum Brain Map, 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
Small, D. M., Jones-Gotman, M., Zatorre, R. J., et al. (1997) Flavor processing: more than the sum of its parts. Neurorep, 8, 3913–17.Google Scholar
Sobel, N., Johnson, B. N., Mainland, J., et al. (2003) Functional neuroimaging of human olfaction. In Handbook of Olfaction and Gustation (ed Doty, R. L.), pp. 461–78. New York: Marcel Dekker, Inc.
Sobel, N., Prabhakaran, V., Desmond, J. E., et al. (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature, 392, 282–6.Google Scholar
Sobel, N., Prabhakaran, V., Hartley, C. A., et al. (1999) Blind smell: brain activation induced by an undetected air-borne chemical. Brain, 122, 209–17.Google Scholar
Sobel, N., Prabhakaran, V., Zhao, et al. (2000) Time course of odorant-induced activation in the human primary olfactory cortex. J Neurophysiol, 83, 537–51.Google Scholar
Talairach, J. & Tournoux, P. (1988) Co-planar stereotaxic atlas of the human brain. New York: Thieme Medic Publishers, Inc.
Trop, D., Olivier., A., Dubeau, F., et al. (1997) Seizure surgery: anesthetic, neurologic, neurosurgical, and neurobehavioral considerations. In Textbook of Neuroanesthesia with Neurosurgical and Neuroscience Perspectives (ed Albin, M. S.), pp. 643–96. New York: McGraw-Hill.
Buren, J. M. (1961) Sensory, motor and autonomic effect of mesial temporal stimulation in man. J Neurosurg, 18, 273–88.Google Scholar
West, S. E. & Doty, R. L. (1995) Influence of epilepsy and temporal lobe resection on olfactory function. Epilepsia, 36, 531–42.Google Scholar
West, S. E., Doty, R. L., O'Conor, M. J., et al. (1993) Pre- and post-operative studies of patients with anterior temporal lobectomy. Cheml Senses, 18, 649.Google Scholar
Wicker, B., Keysers, C., Plailly, J., et al. (2003) Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron, 40, 655–64.Google Scholar
Wilson, D. A. & Sullivan, R. M. (2003) Sensory physiology of central olfactory pathways. In Handbook of Olfaction and Gestation (ed Doty, R. L.), pp. 181–201. New York: Marcel Dekker, Inc.
Wilson, D. A. (1998) Habituation of odor responses in the rat anterior piriform cortex. J Neurophysiol, 79, 1425–40.Google Scholar
Zald, D. H. & Pardo, J. V. (1997) Emotion, olfaction, and the human amygdala: Amygdala activation during aversive olfactory stimulation. Proc Nat Acad Sc USA, 94, 4119–24.Google Scholar
Zald, D. H. & Pardo, J. V. (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol, 36, 165–81.Google Scholar
Zatorre, R. J. & Jones-Gotman, M. (1991) Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain, 114, 71–84.Google Scholar
Zatorre, R. J. & Jones-Gotman, M. (2000) Functional imaging of the chemical senses. In Brain Mapping: The Applications (eds Toga, A. W. & Mazziotta, J. C.), pp. 403–24. San Diego: Academic Press.
Zatorre, R. J. & Jones-Gotman, M., Evans, A., et al. (1992) Functional localization and lateralization of human olfactory cortex. Nature, 360, 339–40.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×