The Impact of Olfaction on Human Social Functioning

doi:10.1017/CBO9780511543623.014

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

Cheryl Corcoran 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

Book contents

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).

Keywords

human emotions human social functioning motivated behaviour neural circuitry schizophrenia sex-specific social function olfaction olfactory systems

Information

Type: Chapter
Information: Olfaction and the Brain , pp. 220 - 232
DOI: https://doi.org/10.1017/CBO9780511543623.014 [Opens in a new window]
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.)

Book purchase

Temporarily unavailable

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

Accessibility standard: Unknown

Why this information is here

This section outlines the accessibility features of this content - including support for screen readers, full keyboard navigation and high-contrast display options. This may not be relevant for you.

Accessibility Information

Accessibility compliance for the PDF of this chapter is currently unknown and may be updated in the future.