Skip to main content Accessibility help
×
Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-26T15:57:17.977Z Has data issue: false hasContentIssue false

12 - The Impact of Olfaction on Human Social Functioning

from Section II - Social Functioning: Role of Evolution, Genetics and Gender

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

Social functioning is key to survival and reproduction across species, as it enables the recognition of self, kin, social status, danger and potential mates. For most mammals, social hierarchy and territory are recognised by odour, and smell plays a key role in identifying conspecifics and enemies, and determining safety from danger. The brain circuitry involved in emotional processing and olfactory function is overlapping, and among sensory modalities, olfaction is unique in that it has direct input to the prefrontal cortex as detailed in Chapter 1. This chapter relates the neurobiology of olfactory processing to social functioning in humans, with a focus on schizophrenia to highlight our understanding of compromise of these processes.

In mammals, social functioning is essential for reproduction and survival, and therefore the neural circuitry and hormonal mechanisms underlying social function are likely to be highly conserved across species (see Insel & Fernald, 2004). Although research on the significance of human olfaction and social communication is nascent, smell is known to play a role in mating, parenting, affiliation and prey–predator relationships in other mammals and it is reasonable to expect an association of the olfactory processing system with social functioning in humans as well. Nonetheless, primates in general (and humans in particular) have decreased olfactory acuity compared to rodents and canine species. Over evolution, as humans developed language and other cognitive processes for socialisation, the selective pressure to maintain olfactory genes for survival and social function was reduced and loss-of-function mutations accumulated in olfactory receptor (OR) genes (Rouquier et al. 2000).

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

Arnold, S. E., Han, L. Y., Moberg, P. J., et al. (2001) Dysregulation of olfactory receptor neuron lineage in schizophrenia. Arch Gen Psychiatry, 58, 829–35.Google Scholar
Bechara, A., Damasio, H., Damasio, A.R. (2000) Emotion, decision making and the orbitofrontal cortex. Cereb cortex, 10, 295–307.
Brewer, W. J., Edwards, J., Anderson, V., et al. (1996) Neuropsychological, olfactory and hygiene deficits in men with negative symptom schizophrenia. Biol Psychiatry, 40, 1021–31.Google Scholar
Brewer, W. J., Pantelis, C., Anderson, V., et al. (2001) Stability of olfactory identification deficits in neuroleptic-naive patients with first-episode psychosis. Am J Psychiatry, 158, 107–15.Google Scholar
Brewer, W. J., Wood, S. J., McGorry, P. D., et al. (2003) Olfactory identification ability is impaired in individuals at ultra high-risk for psychosis who later develop schizophrenia. Am J Psychiatry, 160, 1790–4.Google Scholar
Butter, C. M. & Snyder, D. R. (1972) Alterations in aversive & aggressive behaviors following orbital frontal lesions in rhesus monkeys. Acta Neurobiol Experiment, 32, 525–65.Google Scholar
Carpenter, W. T. Jr., Heinrichs, D. W. & Wagman, A. M. (1988) Deficit and nondeficit forms of schizophrenia: The concept. Am J Psychiatry, 145, 578–83.Google Scholar
Coleman, E., Goetz, R. R., Leitman, D., et al. (2002) Odor identification impairments in schizophrenia: Relationship with demographic measures, clinical variables, and diagnostic subtypes. CNS Spect., 7, 43–8.Google Scholar
Corcoran, C., Whitaker, A., Coleman, E., et al. (2005) Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophr Res, 15, 283–93.
Cowley, J. J. & Brooksbank, B. W. (1991) Human exposure to putative pheromones & changes in aspects of social behaviour. J Steroid Biochem Molec Biol, 39, 647–59.Google Scholar
Damasio, A. R., Tranel, D. & Damasio, H. (1990) Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Beh Brain Res, 41, 81–94.Google Scholar
Doty, R.L., Shaman, P. & Dann, M. (1984) Development of the University of Pennsylvania Smell Identification Test : A standardized microencapsulated test of olfactory function. Physiol Behav, 32, 489–502.
Ehrhardt, A.A., Meyer-Bahlburg, H.F., Rosen, L.R., et al. (1985) Sexual orientation after prenatal exposure to exogenous estrogen. Arch Sex Behav, 14, 57–77.
Frith, C. D. & Frith, U. (1999) Interacting minds—a biological basis. Science, 286, 1692–5.Google Scholar
Gallagher, H. L. & Frith, C. D. (2003) Functional imaging of ‘theory of mind’. Trends Cog Sci, 2, 77–83.Google Scholar
Garcia-Velasco, J. & Mondragon, M. (1992) The incidence of the vomeronasal organ in 1000 human subjects & its possible clinical significance. J Steroid Biochem Molec Biol, 39, 561–3.Google Scholar
Glusman, G., Yanai, I., Rubin, I., et al. (2001) The complete human olfactory subgenome. Genome Res, 11, 685–702.Google Scholar
Grammer, K. & Jutte, A. (1997) Battle of odors: significance of pheromones for human reproduction. Gynakol Geburtshilfliche Rundsch, 37, 150–3.Google Scholar
Gusnard, D. A., Akbudak, E., Shulman, G. L., et al. (2001) Medial prefrontal cortex & self-referential mental activity: relation to a default mode of brain function. Proc Nat Acad Sci USA, 98, 4259–64.Google Scholar
Gustavson, A. R., Dawson, M. E. & Bonett, D. G. (1987) Androstenol, a putative human pheromone, affects human (Homo sapiens) male choice performance. J Comp Psychol, 101, 210–12.Google Scholar
Haqq, C. M., King, C. Y., Ukiyama, E., et al. (1994) Molecular basis of mammalian sexual determination: activation of Mullerian inhibiting substance gene expression by SRY. Science, 266, 1494–500.Google Scholar
Harlow, J. M. (1868) Recovery of the passage of an iron bar through the head. Pub Mass Med Soc, 2, 327–47.Google Scholar
Houlihan, D. J., Flaum, M., Arnold, S. E., et al. (1994) Further evidence for olfactory identification deficits in schizophrenia. Schizophr Res, 12, 179–82.Google Scholar
Hurwitz, T., Kopala, L., Clark, C., et al. (1988) Olfactory deficits in schizophrenia. Biol Psychiatry, 23, 123–8.Google Scholar
Insel, T. R. & Fernald, R. (2004) How the brain processes social information: searching for the social. Ann Rev Neurosci, 27, 697–722.Google Scholar
James, W. (1950) The Principles of Psychology, Volumes 1, 2. New York: [reprinted 1950], Dover 1890.
Kandel, E. (2000) Principles of Neural Science. (eds Schwartz, J. H. & Jessell, T. M.), pp. 513–29. New York: Elsevier.
Kemperman, G., Praag, H. & Gage, F. (2000) Activity-dependent regulation of neuronal plasticity and self-repair. Prog Brain Res, 127, 35–48.Google Scholar
Kirkpatrick, B., Buchanan, R. W., McKenney, P. D., et al. (1989) The Schedule for the Deficit Syndrome: an instrument for research in schizophrenia. Psychiatry Res, 30, 119–23.Google Scholar
Kirkpatrick, B., Buchanan, R. W., Ross, D. E., et al. (2001) A separate disease within the syndrome of schizophrenia. Arch Gen Psychiatry, 58, 165–70.Google Scholar
Kjaer, I. & Hansen, B. F. (1996) Luteinizing hormone-releasing hormone & innervation pathways in human prenatal nasal submucosa: factors of importance in evaluating Kallmann's syndrome. APMIS, 104, 680–8.Google Scholar
Kohl, J. V. (2001) Human Pheromones: Integrating Neuroendocrinology & Ethology. (eds Atzmueller, M., Fink, B. & Grammer, K.) Neuroendocr Letters, 22, 319–32.
Kopala, L. C. & Good, K. P. (1996) Olfactory identification ability in patients with panic disorder. J Psychiatry Neurosci, 21, 340–2.Google Scholar
Kopala, L., Good, K., Martzke, J., et al. (1995) Olfactory deficits in schizophrenia are not a function of task complexity. Schizophr Res, 17, 195–9.Google Scholar
Kopala, L., Good, K. P., Torrey-Fuller, E., et al. (1997) Olfactory function in monozygotic twins discordant for schizophrenia. Biol Psychiatry, 42, 194S.Google Scholar
Kopala, L. C., Good, K. P., Morrison, K., et al. (2001) Impaired olfactory identification in relatives of patients with familial schizophrenia. Am J Psychiatry, 158, 1286–90.Google Scholar
Licht, G. & Meredith, M. (1987) Convergence of main & accessory olfactory pathways onto single neurons in the hamster amygdala. Exp Brain Res, 69, 7–18.Google Scholar
Malaspina, D. & Coleman, E. (2003) Olfaction and social drive in schizophrenia. Arch Gen Psychiatry, 60, 578–84.Google Scholar
Malaspina, D., Wray, A. D., Friedman, J. H., et al. (1994) Odor discrimination deficits in schizophrenia: Associations with eye movement dysfunction. J Neuropsychology Clin Neurosci, 6, 273–8.Google Scholar
Malaspina, D., Perera, G. M., Lignelli, A., et al. (1998) SPECT imaging of odor identification in schizophrenia. Psychiatry Res, 82, 53–61.Google Scholar
Malaspina, D., Goetz, R. R. & Yale, S. (2000) Relation of familial schizophrenia to negative symptoms but not to the deficit syndrome. Am J Psychiatry, 157, 994–1003.Google Scholar
Martzke, J. S., Kopala, L. C. & Good, K. P. (1997) Olfactory dysfunction in neuropsychiatric disorders: review and methodological considerations. Biol Psychiatry, 42, 721–32.Google Scholar
Matsumoto, A. & Arai, Y. (1986) Development of sexual dimorphism in synaptic organization in the ventromedial nucleus of the hypothalamus in rats. Neurosci Letters, 68, 165–8.Google Scholar
Meyer-Bahlburg, H. F., Ehrhardt, A. A. & Feldman, J. F. (1985) Sexual activity level & sexual functioning in women prenatally exposed to diethylstilbestrol. Psychosom Med, 47, 97–511.Google Scholar
Moberg, P. J., Agrin, R., Gur, R. E., et al. (1999) Olfactory dysfunction in schizophrenia: A qualitative and quantitative review. Neuropsychopharmacology, 21, 25–340.Google Scholar
Moran, D. T., Jafek, B. W. & Rowley, J. C. III (1991) The vomeronasal (Jacobson's) organ in man: ultrastructure & frequency of occurrence. J Ster Biochem Molec Biol, 39, 545–52.Google Scholar
Morofushi, M., Shinohara, K., Funabashi, T., et al. (2000) Positive relationship between menstrual synchrony & ability to smell 5alpha-androst-16-en-3alpha-ol. Chem Senses, 25, 407–11.Google Scholar
Myers, R. E., Swett, C. & Miller, M. (1973) Loss of social group affinity following prefrontal lesions in free-ranging macaques. Brain Res, 64, 257–69.Google Scholar
Naftolin, F., Harris, G. W. & Bobrow, M. (1971) Effect of purified luteinizing hormone releasing factor on normal & hypogonadotrophic anosmic men. Nature, 232, 496–7.Google Scholar
Nauta, W. H. J. (1971) The problem of the frontal lobe: a reinterpretation. J Psychiatry Res, 8, 167–87.Google Scholar
Nordeen, E. J., Nordeen, K. W., Sengelaub, D. R., et al. (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science, 229, 671–3.Google Scholar
Öngür, D. & Price, J. L. (2000) The organization of networks within the orbital & medial prefrontal cortex of rats, monkeys & humans. Cereb Cortex, 10, 206–19.Google Scholar
Park, S. & Schoppe, S. (1997) Olfactory identification deficit in relation to schizotypy. Schizophr Res, 26, 191–7.Google Scholar
Porter, R. H. & Winberg, J. (1999) Unique salience of maternal breast odor for newborns. Neurosci Biobehav Rev, 23, 439–49.Google Scholar
Purdon, S. E. (1998) Olfactory identification and Stroop interference converge in schizophrenia. J Psychiatric Neurosci, 23, 163–71.Google Scholar
Rouquier, S., Blancher, A. & Giorgi, D. (2000) The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc Nat Acad Sci USA, 14, 2870–4.Google Scholar
Rubin, B. S., Mitchell, S., Lee, C. E., et al. (1995) Reconstructions of populations of luteinizing hormone releasing hormone neurons in young and middle-aged rats reveal progressive increases in subgroups expressing Fos protein on proestrus and age-related deficits. Endocrinol, 136, 3823–30.Google Scholar
Rugarli, E. I. & Ballabio, A. (1993) Kallmann syndrome. From genetics to neurobiology. JAMA, 270, 2713–6.Google Scholar
Schaal, B. (1995) Odor sensing in the human fetus: Anatomical, functional, & chemeo-ecological Bases. In Fetal Development: A Psychobiological Perspective (eds Orgeur, P. & Rognon, C.), pp. 205–37. Hillsdale, NJ, Lawrence Erlbaum Associate.
Schachter, S. & Singer, J. (1962) Cognitive, social & physiological determinants of emotional state. Psycholog Rev, 69, 379–99.Google Scholar
Schleidt, M. & Genzelm, C. (1990) The significance of mother's perfume for infants in the first few weeks of their life. Ethol Sociobiol, 11, 145–54.Google Scholar
Segovia, S. & Guillamon, A. (1993) Sexual dimorphism in the vomeronasal pathway & sex differences in reproductive behaviors. Brain Res Rev, 18, 51–74.Google Scholar
Stensaas, L. J., Lavker, R. M., Monti-Bloch, L., et al. (1991) Ultrastructure of the human vomeronasal organ. J Steroid Biochem Molec Biol, 39, 553–60.Google Scholar
Stern, K. & McClintock, M. K. (1998) Regulation of ovulation by human pheromones. Nature, 392, 177–9.Google Scholar
Striebel, K. M., Beyerstein, B., Remick, R. A., et al. (1999) Olfactory identification and psychosis. Biol Psychiatry, 45, 1419–25.Google Scholar
Sullivan, R. M.., Mendoza, R., et al. (1991) Olfactory classical conditioning in neonates. Pediatrics, 87, 511–18.Google Scholar
Swann, J. & Fiber, J. M. (1997) Sex differences in function of a pheromonally stimulated pathway: role of steroids & the main olfactory system. Brain Res Bull, 44, 409–13.Google Scholar
Tobet, S. A. & Fox, T. O. (1989) Sex- & hormone-dependent antigen immunoreactivity in developing rat hypothalamus. Proc Nat Acad Sci USA, 86, 382–6.Google Scholar
Toller, C., Kirk-Smith, M., Wood, N., et al. (1983) Skin conductance and subjective assessments associated with the odour of 5-alpha-androstan-3-one. Biol Psychology, 16, 85–107.Google Scholar
Wedekind, C., Seebeck, T., Bettens, F., et al. (1995) MHC-dependent mate preferences in humans. Proc Royal Soc Lond, 260, 245–9.Google Scholar
Wysocki, C. J. & Beauchamp, G. K. (1984) Ability to smell androstenone is genetically determined. Proc Natl Acad Sci USA, 81, 4899–902.
Zald, D. H. & Pardo, J. V. (1997) Emotion, olfaction, & the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA, 94, 4119–24.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
×