Abstract
The current report used structural magnetic resonance imaging (MRI) to objectively measure olfactory bulb volume and olfactory sulcal depth in patients diagnosed with chronic schizophrenia and healthy controls. Additional measures were obtained to assess olfactory function. The olfactory bulb and sulcus were manually traced on structural 3T MRIs for 25 right-handed male patients diagnosed with chronic schizophrenia and 25 matched male healthy controls. A sub-set of subjects received the University of Pennsylvania Smell Identification Test (UPSIT). Olfactory bulb volume was significantly decreased in patients with schizophrenia compared to healthy controls, as was their performance on the UPSIT. Additionally, a positive correlation was seen in patients between right bulb volume and UPSIT scores. Overall, our findings support earlier research studies showing morphometric and functional changes in the olfactory system in patients with schizophrenia.
Similar content being viewed by others
References
Abolmaali, N. D., Hietschold, V., Vogl, T. J., Huttenbrink, K. B., & Hummel, T. (2002). MR evaluation in patients with isolated anosmia since birth or early childhood. American Journal of Neuroradiology, 23, 157–163.
Amsterdam, J. D., Settle, R. G., Doty, R. L., Abelman, E., & Winokur, A. (1987). Taste and smell perception in depression. Biological Psychiatry, 22, 1481–1485.
Andreasen, N. C. (1983). The scale for the assessment of negative symptoms (SANS). Iowa: The University of Iowa.
Andreasen, N. C. (1984). The scale for the assessment of positive symptoms (SAPS). Iowa: The University of Iowa.
Bellas, D. N., Novelly, R. A., & Eskanazi, B. (1989). Olfactory lateralization and identification in right hemisphere lesions and control patients. Neuropsychologia, 9, 1187–1191.
Brewer, W. J., Pantelis, C., Anderson, V., Velakoulis, D., Singh, B., Copolov, D. L., et al. (2001). Stability of olfactory identification deficits in neuroleptic-naïve patients with first-episode psychosis. The American Journal of Psychiatry, 158, 107–115.
Brewer, W. J., Wood, S. J., McGorry, P. D., Francey, S. M., Phillips, L. J., Yung, A. R., et al. (2003). Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. The American Journal of Psychiatry, 160, 1970–1794.
Crespo-Facorro, B., Kim, J., Andreasen, N. D., O’Leary, D. S., Watkins, G. L., Ponto, L. L., et al. (2001). Neural mechanisms of anhedonia in schizophrenia: a PET study of response to unpleasant and pleasant odors. JAMA, 286, 427–435.
First, M. B., Spitzer, R. L., Gibbon, M., Williams, J. B. W., Davies, M., Borus, J., et al. (1995). The structured clinical interview for DSM-III-R personality disorders (SCID-II). Part II: multi-site test-retest reliability study. Journal of Personality Disorders, 9(2), 92–104.
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1997). Structured clinical interview for DSM-IV axis I disorders-clinician version (SCID-CV). American Psychiatric Press.
Frye, R. E., Schwartz, B. S., & Doty, R. L. (1990). Dose-related effects of cigarette smoking on olfactory function. Journal of the American Medical Association, 263(9), 1233–1236.
Fulbright, R. K., Skudlarski, P., Lacadie, C. M., et al. (1998). Functional MR imaging of regional brain responses to pleasant and unpleasant odors. AJNR. American Journal of Neuroradiology, 19, 1721–1726.
Good, K. P., Martzke, J. S., Honer, W. G., & Kopala, L. C. (1998). Left nostril identification impairment in a subgroup of male patients with schizophrenia. Schizophrenia Research, 33, 35–43.
Heaton, R. K. (1981). Wisconsin card sorting test, manual. Odessa: Psychological Assessment Resources.
Heine, O., & Galaburda, A. M. (1986). Olfactory asymmetry in the rat brain. Experimental Neurology, 91, 392–398.
Hollingshead, A. B. (1965). Two factor index of social position. New Haven: Yale University. Unpublished manuscript.
Hummel, T., Damm, M., Vent, J., Schmidt, M., Theissen, P., Larsson, M., et al. (2003). Depth of olfactory sulcus and olfactory function. Brain Research, 975, 85–89.
Hurtwitz, T., Kopala, L., Clark, C., & Jones, B. (1988). Olfactory deficits in schizophrenia. Biological Psychiatry, 23, 123–128.
Jones-Gotman, M., & Zatorre, R. J. (1993). Odor recognition memory in humans: role of right temporal and orbitofrontal regions. Brain and Cognition, 22, 182–198.
Katotomichelakis, M., Balatsouras, D., Tripsianis, G., Gavris, S., Marondias, N., Danielides, V., et al. (2007). The effect of smoking on the olfactory function. Rhinology, 45(4), 273–280.
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261–276.
Kopala, L., & Clark, C. (1990). Implications of olfactory agnosia for understanding sex differences in schizophrenia. Schizophrenia Bulletin, 16(2), 255–261.
Kopala, L., Clark, C., & Hurwitz, T. A. (1993). Olfactory deficits in neuroleptic naïve patients with schizophrenia. Schizophrenia Research, 8, 245–250.
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, 205–211.
Kopala, L. C., Good, K., Goldner, E. M., & Birmingham, C. L. (1995). Olfactory identification ability in anorexia nervosa. Journal of Psychiatry & Neuroscience, 20, 283–286.
Kopala, L., Good, K., Martzke, J., & Hurwitz, T. (1995). Olfactory deficits in schizophrenia is not a function of task complexity. Schizophrenia Research, 17, 195–199.
Kopala, L. C., Good, K. P., Morrison, K., Bassett, A. S., Alda, M., & Honer, W. G. (2001). Impaired olfactory identification in relatives of patients with familial schizophrenia. The American Journal of Psychiatry, 158, 1286–1290.
Lezak, M. D. (1995). Neuropsychological assessment (3rd ed.). Oxford: Oxford University Press.
Mesholam, R. I., Moberg, P. J., Mahr, R. N., & Doty, R. L. (2001). Olfaction in neurodegenerative disease. A meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Archives of Neurology, 55, 84–90.
Moberg, P. J., Agrin, R., Gur, R. E., Gur, R. C., Turetsky, B. I., & Doty, R. L. (1999). Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology, 21, 325–340.
Moberg, P. J., Arnold, S. E., Doty, R. L., Gur, R. E., Basderston, C. C., & Roalf, D. R. (2006). Olfactory functioning in schizophrenia: relationship to clinical, neuropsychological, and volumetric MRI measures. Journal of Clinical and Experimental Neuropsychology, 28, 1444–1461.
Negoias, S., Croy, I., Gerver, J., Puschmann, S., Petrowski, J., & Hummel, T. (2010). Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience, 169, 415–421.
Nestor, P. G., Shenton, M. E., McCarley, R. W., Haimson, J., Smith, R. S., O’Donnell, B., et al. (1993). Neuropsychological correlates of MRI temporal lobe abnormalities in schizophrenia. The American Journal of Psychiatry, 150(12), 1849–1855.
Nguyen, A. D., Shenton, M. E., & Levitt, J. J. (2010). Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harvard Review of Psychiatry, 18(5), 279–292.
Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97–113.
Reitan, R., & Wolfson, D. (1985). The halstead-reitan neuropsychological test battery. Tucson: Neuropsychology Press.
Rombaux, P. H., Potier, H., Markessis, E., Dupez, T., & Hummel, T. (2010). Olfactory bulb volume and depth of olfactory sulcus in patients with idiopathic olfactory loss. European Archives of Otorhinolaryngology, 10, 1551–1556.
Rupp, C. I. (2003). Dysfunction in olfactory processing in schizophrenia. Current Opinion in Psychiatry, 16, 181–185.
Rupp, C. I., Fleischhacker, W. W., Kemmler, G., Oberbauer, H., Wcholtz, A. R., Wanko, C., et al. (2005). Various bilateral olfactory deficits in male patients with schizophrenia. Schizophrenia Bulletin, 31(1), 155–165.
Seidman, L. J., Talbot, N. L., Kalinowki, A. G., McCarley, R. W., & Tsuang, M. T. (1992). Neuropsychological probes of fronto-limbic system dysfunction in schizophrenia: olfactory identification and wisconsin card sorting performance. Schizophrenia Research, 6, 55–65.
Skosnik, P. D., Spatz-Glenn, L., & Park, S. (2001). Cannabis use is associated with schizotypy and attentional disinhibition. Schizophrenia Research, 48, 83–92.
Sobel, N., Khan, R. M., Saltman, A., Sullivan, E. V., & Gabrieli, J. D. (1999). The world smells different to each nostril. Nature, 402, 35.
Tulsky, D. S., Saklofske, D. H., Wilkins, C., & Weiss, L. G. (2001). Development of a general ability index for the wechsler adult intelligence scale. Psychological Assessment, 13(4), 566–571.
Turetsky, B. I., & Moberg, P. J. (2009). An odor specific threshold deficit implicates abnormal intracellular cyclic-AMP signaling in schizophrenia. The American Journal of Psychiatry, 166, 226–233.
Turetsky, B. I., Moberg, P. J., Youse, D. M., Doty, R. L., Arnold, S. E., & Gur, R. E. (2000). Reduced olfactory bulb volume in patients with schizophrenia. The American Journal of Psychiatry, 157, 828–830.
Turetsky, B. I., Moberg, P. J., Arnold, S. E., Doty, R. L., & Gur, R. E. (2003). Low olfactory bulb volume in first-degree relatives of patients with schizophrenia. The American Journal of Psychiatry, 160, 703–708.
Turetsky, B. I., Moberg, P. J., Owzar, K., Johnson, S. C., Doty, R. L., & Gur, R. E. (2003). Physiologic impairment of olfactory stimulus processing in schizophrenia. Biological Psychiatry, 53, 403–411.
Turetsky, B. I., Crutchley, P., Walker, J., Gur, R. E., & Moberg, P. J. (2009). Depth of olfactory sulcus: a marker of early embryonic disruption in schizophrenia? Schizophrenia Research, 115(1), 8–11.
Turetsky, B. I., Curtchley, P., Walker, J., Gur, R. E., & Moberg, P. J. (2009). Scents and nonsense: olfactory dysfunction in schizophrenia. Schizophrenia Bulletin, 35(6), 1117–1131.
Turetsky, B. I., Hahn, C. G., Arnold, S. E., & Moberg, P. J. (2009). Olfactory receptor neuron dysfunction in schizophrenia. Neuropsychopharmacology, 34(3), 767–774.
Wechsler, D. (1997). Wechsler memory scale (3rd ed.). Brace: Harcourt.
Wilkinson, G. S. (1993). The wide range achievement test: manual (3rd ed.). Wilmington: Wide Range.
Wu, J., Buchsbaum, M. S., Moy, K., Denlea, N., Kesslak, P., Tseng, H., et al. (1993). Olfactory memory in unmedicated schizophrenics. Schizophrenia Research, 9, 41–47.
Yousem, D. M., Geckle, R. J., Bilker, W. B., & Doty, R. L. (1998). Olfactory bulb and rat and temporal lobe volumes: normative data across decades. Annual N Y Academy Science, 855, 546–555.
Zatorre, R. J., Jones-Gotman, M., Evans, A. C., & Meyer, E. (1992). Functional localization and lateralization of human olfactory cortex. Nature, 360, 339–340.
Acknowledgment
We wish to thank Jorge Alvorado BS for his work with the olfactory sulcus reliability and tracing procedure and Fawad Taj, MD for his work on reliability with the olfactory sulcus. We also wish to thank Doug Terry BA for his advice on biostatistics, as well as Lindsay F Morra BA, Jenna M Mezin, BA and Shannon Sorenson, BA for their work with administering the UPSIT tests.
This work was supported in part by VA Merit Awards (JJL, MES, RWM), by a VA Schizophrenia Center Grant (RWM, MES), by a K05 Award supported by the National Institute of Mental Health (MH 070047 to MES), by an R01 Award supported by the National Institute of Mental Health (MH 50740 to MES), and by support from an NIH Mental Health Center for Clinical Interventional Development and Applied Research (P50 11P50 MH 080272; RWM, MES).
Disclosure
The authors of this empirical paper report no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Authorship: The authors affirm having had full access to all data from the study; both from what is reported and what is unreported, and also that the authors had complete freedom to direct this study’s analysis and reporting, without influence from the sponsors. The corresponding authors also affirm that there was no editorial direction or censorship from any sponsors.
Statement: This empirical article represents original materials, it has not been previously published, and it is not under consideration for publication elsewhere.
Rights and permissions
About this article
Cite this article
Nguyen, A.D., Pelavin, P.E., Shenton, M.E. et al. Olfactory sulcal depth and olfactory bulb volume in patients with schizophrenia: an MRI study. Brain Imaging and Behavior 5, 252–261 (2011). https://doi.org/10.1007/s11682-011-9129-0
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-011-9129-0