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Neuropsychological Characteristics Associated with Olfactory Hallucinations in Schizophrenia

Published online by Cambridge University Press:  22 May 2012

Deborah Arguedas ,
Robyn Langdon  and
Richard Stevenson
Deborah Arguedas
Affiliation:
Psychology Department, Macquarie University, Sydney, New South Wales, Australia ARC Centre of Excellence in Cognition and Its Disorders, Department of Cognitive Science, Macquarie University, Sydney, Australia
Robyn Langdon*
Affiliation:
ARC Centre of Excellence in Cognition and Its Disorders, Department of Cognitive Science, Macquarie University, Sydney, Australia
Richard Stevenson
Affiliation:
Psychology Department, Macquarie University, Sydney, New South Wales, Australia
*
Correspondence and reprint requests to: Robyn Langdon, ARC Centre of Excellence in Cognition and Its Disorders, Department of Cognitive Science, Macquarie University, Sydney, NSW 2019, Australia. E-mail: [email protected]
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Abstract

Olfactory hallucinations (OHs) are present in a significant minority of people with schizophrenia, yet these symptoms are under-researched and poorly understood. This study aimed to identify the neuropsychological impairments that associate with OHs in schizophrenia. Patients with schizophrenia or schizoaffective disorder were classified into an OH group and a group with auditory-verbal hallucinations (AVHs) and no lifetime history of OHs. Patients were age- and gender-matched to a healthy control group. All participants were assessed using: a test of odor identification; decision-making and socio-emotional tests of orbitofrontal cortex (OFC) and amygdala function; and a battery of standardized executive tests. Patients, as a whole, performed more poorly than controls on the tests of odor identification, emotion processing and executive function, consistent with previous research. Only two tests of OFC functioning: the Object Alternation Task, taken from Oscar-Berman and Zola-Morgan's (1980a, 1980b) Comparative Neuropsychological Tasks, and a test of “faux pas” understanding discriminated between the OH and AVH patients. Findings provide the first preliminary support for OH-specific neuropsychological impairments associated with OFC dysfunction in schizophrenia. (JINS, 2012, 18, 1–10)

Keywords

HallucinationsSchizophrenia spectrumOlfactory processingPsychosisOrbitofrontal functionAmygdala function
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 5 , September 2012 , pp. 799 - 808
Copyright
Copyright © The International Neuropsychological Society 2012

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References

Acharya, V., Acharya, J., Luders, H. (1998). Olfactory epileptic auras. Neurology, 51, 56–61.Google Scholar
Adolphs, R., Baren-Cohen, S., Tranel, D. (2002). Impaired recognition of social emotions following amygdale damage. Journal of Cognitive Neuroscience, 14, 1264–1274.CrossRefGoogle Scholar
Adolphs, R., Tranel, D. (2003). Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions. Neuropsychologia, 41, 1281–1289.CrossRefGoogle ScholarPubMed
Andreasen, N.G. (1984a). Scale for the assessment of negative symptoms (SANS). Iowa City: University of Iowa Press.Google Scholar
Andreasen, N.G. (1984b). Scale for the assessment of positive symptoms (SAPS). Iowa City: University of Iowa Press.Google Scholar
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., Plumb, I. (2001). The “Reading the mind in the eyes” Test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, 42, 241–251.CrossRefGoogle ScholarPubMed
Bell, E.M., Langdon, R., Siegert, R.J., Ellis, P.M. (2010). The assessment of Theory of Mind in schizophrenia. In G. Dimaggio & P.H. Lysaker (Eds.), Metacognition and severe adult mental disorders: From research to treatment (pp. 115–133). London: Routledge Press.Google Scholar
Blumenfeld, H. (2002). Neuroanatomy through clinical cases. Sunderland, MA: Sinauer Associates, Inc.Google Scholar
Bora, E., Yucel, M., Pantelis, C. (2009). Theory of mind impairment in schizophrenia: Meta-analysis. Schizophrenia Research, 109, 1–9.Google Scholar
Carmichael, S.T., Clugnet, M.C., Price, J.J. (1994). Central olfactory connections in macaque monkeys. Journal of Comparative Neurology, 346, 403–434.CrossRefGoogle Scholar
Castle, D.J., Jablensky, A., McGrath, J.J., Carr, V., Morgan, V., Waterreus, A., Farmer, A. (2006). The diagnostic interview for psychoses (DIP): Development, reliability and applications. Psychological Medicine, 36, 69–80.CrossRefGoogle ScholarPubMed
Chen, C., Shih, Y.-H., Yen, D.-J., Lirng, J.-F., Guo, Y.-C., Yu, H.-Y., Yiu, C.-H. (2003). Olfactory auras in patients with temporal lobe epilepsy. Epilepsia, 44, 257–260.CrossRefGoogle ScholarPubMed
Chitanondh, H. (1966). Sterotaxic amygdalotomy in the treatment of olfactory seizures and psychiatric disorders with olfactory hallucinations. Confinia Neurologica, 27, 181–196.Google Scholar
Crowder, R.G., Schab, F.R. (1995). Imagery for odors. In F.R. Schab & R.G. Crowder (Eds.), Memory for odors (pp. 93–107). Mahwah, NJ: L Erlbaum Associates.Google Scholar
Delisi, L.E. (1992). The significance of age of onset for schizophrenia. Schizophrenia Bulletin, 18, 209–215.CrossRefGoogle ScholarPubMed
Doty, R.L. (1989). The Smell Identification Test Administration Manual. Haddon Heights, NJ: Sensonics Inc.Google Scholar
Edwards, J., Jackson, H.J., Pattison, P.E. (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: A methodological review. Clinical Psychology Review, 22, 789–832.CrossRefGoogle ScholarPubMed
Ekman, P., Friesen, W.V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
First, M.B., Spitzer, R.L., Gibbon, M., Williams, J.B.W. (1996). Structured Clinical Interview for DSM-IV Axis I Disorders-Patient Edition (SCID-I/P, Version 2.0). New York: New York State Psychiatric Institute, Biometrics Research Department.Google Scholar
Freedman, M. (1990). Object alternation and orbitofrontal system in Alzheimer's and Parkinson's disease. Brain and Cognition, 14, 134–143.Google Scholar
Freedman, M., Black, S., Ebert, P., Binns, M. (1998). Orbitofrontal function, object, alternation and perseveration. Cerebral Cortex, 8(1), 18–27.CrossRefGoogle ScholarPubMed
Fuller, G.N., Guiloff, R.J. (1987). Migrainous olfactory hallucinations. Journal of Neurology, Neurosurgery, and Psychiatry, 50, 1688–1690.CrossRefGoogle ScholarPubMed
Gogtay, N., Vyas, N.S., Testa, R., Wood, S.J., Pantelis, C. (2011). Age of onset of schizophrenia: Perspectives from structural neuroimaging studies. Schizophrenia Bulletin, 37, 504–513.Google Scholar
Gallagher, S., Frith, C.D. (2003). “Functional imaging of ‘theory of mind’”. Trends in Cognitive Sciences, 7, 77–83.CrossRefGoogle Scholar
Gellermann, L.W. (1933). Chance orders of alternating stimuli in visual discrimination tasks. Journal of Genetic Psychology, 42, 206–208.Google Scholar
Green, M.J., Williams, L.M., Davidson, D. (2003). Visual scanpaths to threat-related faces in deluded schizophrenia. Psychiatry Research, 119, 271–285.CrossRefGoogle ScholarPubMed
Gregory, C., Lough, S., Stone, V., Erzinclioglu, S., Martin, L., Baron-Cohen, S., Hodges, J.R. (2002). Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer's disease: Theoretical and practical implications. Brain, 125, 752–764.CrossRefGoogle ScholarPubMed
Hawkes, C.H., Doty, R.L. (2009). The neurology of olfaction. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Heinrichs, R., Zakzanis, K.K. (1998). Neurocognitive deficit in schizophrenia: A quantitative review of the evidence. Neuropsychology, 12(3), 426–445.CrossRefGoogle ScholarPubMed
Herz, R.S. (2000). Verbal coding in olfactory versus nonolfactory cognition. Memory and Cognition, 28, 957–964.Google Scholar
Kay, S.R., Opler, L.A., Spitzer, R.L., Williams, J.B.W., Fiszbein, A., Gorelick, A. (1991). SCIDPANSS: Two-tier diagnostic system for psychotic disorders. Comprehensive Psychiatry, 32, 355–361.CrossRefGoogle ScholarPubMed
Kang, N., Baum, M.J., Cherry, J.A. (2009). A direct main olfactory bulb projection to the ‘vomeronasal’ amygdale in female mice selectively responds to volatile pheromones from males. European Journal of Neuroscience, 29, 624–634.CrossRefGoogle Scholar
Kohler, C., Brennan, A. (2004). Recognition of facial emotions in schizophrenia. Current Opinion in Psychiatry, 17, 81–86.Google Scholar
Kopala, L.C., Good, K.P., Honer, W.G. (1994). Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophrenia Research, 12(3), 205–211.CrossRefGoogle ScholarPubMed
Kwapil, T.R., Chapman, J.P., Chapman, L.J., Miller, M.B. (1996). Deviant olfactory experiences as indicators of risk for psychosis. Schizophrenia Bulletin, 22, 371–382.Google Scholar
Langdon, R. (2005). Theory of mind in schizophrenia. In B. Malle & S. Hodges (Eds.), Other minds; How humans bridge the divide between self and others (pp. 323–342). New York: Guilford Press.Google Scholar
Langdon, R., Coltheart, M., Ward, P.B. (2006). Empathetic perspective-taking is impaired in schizophrenia: Evidence from a study of emotion attribution & theory of mind. Cognitive Neuropsychiatry, 11(2), 133–155.CrossRefGoogle ScholarPubMed
Langdon, R., Coltheart, M., Ward, P.B. (2010). Reasoning anomalies associated with delusions in schizophrenia. Schizophrenia Bulletin, 36, 321–330.CrossRefGoogle ScholarPubMed
Langdon, R., McGuire, J., Stevenson, R., Catts, S.V. (2011). Clinical correlates of olfactory hallucinations in schizophrenia. British Journal of Clinical Psychology, 50, 145–163.CrossRefGoogle ScholarPubMed
Lewandowski, K.E., DePaola, J., Camsari, G.B., Cohen, B.M., Öngür, D. (2009). Tactile, olfactory, and gustatory hallucinations in psychotic disorders: A descriptive study. Annals of the Academy of Medicine, Singapore, 38, 383–387.Google Scholar
Meats, P. (1988). Olfactory hallucinations. British Medical Journal, 296, 645.Google Scholar
Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N.R., Luo, L. (2011). Cortical representations of olfactory input by trans-synaptic tracing. Nature, 472, 191–196.Google Scholar
Oscar-Berman, M., Bardenhagen, F. (1998). Nonhuman animal models of memory dysfunction in neurodegenerative disease (pp. 3–20). NY: Cambridge University Press.Google Scholar
Oscar-Berman, M., Zola-Morgan, S.M. (1980a). Comparative neuropsychology and Korsakoff's Syndrome I-spatial and visual reversal learning. Neuropsychologia, 18, 499–512.CrossRefGoogle ScholarPubMed
Oscar-Berman, M., Zola-Morgan, S.M. (1980b). Comparative neuropsychology and Korsakoff's Syndrome II-two-choice visual discrimination learning. Neuropsychologia, 18, 513–525.CrossRefGoogle ScholarPubMed
Pantelis, C., Brewer, W. (1995). Neuropsychological and olfactory dysfunction in schizophrenia: Relationship of frontal syndromes to syndromes of schizophrenia. Schizophrenia Research, 17(1), 35–45.Google Scholar
Pantelis, C., Yucel, M., Wood, S.J., Velakoulis, D., Sun, D., Berger, G., McGorry, P.D. (2005). Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. Schizophrenia Bulletin, 31, 672–696.CrossRefGoogle ScholarPubMed
Reichenberg, A., Harvey, P.D. (2007). Neuropsychological impairments in schizophrenia: Integration of performance-based and brain imaging findings. Psychological Bulletin, 133(5), 833–858.Google Scholar
Saoud, M., Hueber, T., Mandran, H., Dalery, J., d'Amato, T. (1998). Olfactory identification deficiency and WCST performance in men with schizophrenia. Psychiatry Research, 81(2), 251–257.CrossRefGoogle ScholarPubMed
Saxe, R., Kanwisher, N. (2003). People thinking about thinking people: The role of the temporo-parietal junction in “theory of mind”. Neuroimage, 19, 1835–1842.CrossRefGoogle ScholarPubMed
Schreiber, A., Calvert, P.C. (1986). Migrainous olfactory hallucinations. Headache, 26, 513–514.CrossRefGoogle ScholarPubMed
Seal, M.L., Aleman, A., McGuire, P. (2004). Compelling imagery, unanticipated speech and deceptive memory: Neurocognitive models of auditory verbal hallucinations in schizophrenia. Cognitive Neuropsychiatry, 9(1/2), 43–72.Google Scholar
Seidman, L.J., Oscar-Berman, M., Kalinowski, A.G., Ajilore, O., Kremen, W.S., Faraone, S.V., Tsuang, M.T. (1995). Experimental and clinical neuropsychological measures of prefrontal dysfunction in schizophrenia. Neuropsychology, 9(4), 481–490.CrossRefGoogle Scholar
Shenton, M.E., Dickey, C.C., Frumin, M., McCarley, R.W. (2001). A review of MRI findings in schizophrenia. Schizophrenia Research, 49, 1–52.Google Scholar
Shaw, P., Bramham, J., Lawrence, E.J., Morris, R., Baron-Cohen, S., David, A.S. (2005). Differential effects of lesions of the amygdala and prefrontal cortex on recognizing facial expressions of complex emotions. Journal of Cognitive Neuroscience, 17, 1410–1419.Google Scholar
Stedman, T.J., Clair, A.L. (1998). Neuropsychological, neurological and symptom correlates of impaired olfactory identification in schizophrenia. Schizophrenia Research, 32(1), 23–30.Google Scholar
Stevenson, R., Langdon, R., McGuire, J. (2011). Olfactory hallucinations in schizophrenia and schizoaffective disorder: A phenomenological survey. Psychiatry Research, 185, 321–327.Google Scholar
Stone, V.E., Baron-Cohen, S., Calder, A., Keane, J., Young, A. (2003). Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia, 41(2), 209–220.Google Scholar
Stone, V.E., Baron-Cohen, S., Knight, R.T. (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience, 10(5), 640–656.CrossRefGoogle ScholarPubMed
Torralva, T., Kipps, C.M., Hodges, J.R., Clark, L., Bekinschtein, T., Roca, M., Manes, F. (2007). The relationship between affective decision-making and theory of mind in the frontal variant of fronto-temporal dementia. Neuropsychologia, 45, 342–349.Google Scholar
Velakoulis, D. (2006). Olfactory hallucinations. In W.J. Brewer, D. Castle, C. Pantelis (Eds.), Olfaction and the brain (pp. 322–333). Melbourne: CUP.Google Scholar
Wechsler, D. (2001). Wechsler Test of Adult Reading. USA: Psychological Corporation.Google Scholar