Olfactory dysfunction in schizophrenia: A review of neuroanatomy and psychophysiological measurements

Harvard Review of Psychiatry

Volumn 18, Issue 5, 2010, Pages 279-292

  Nguyen, An D ^b   Shenton, Martha E ^b   Levitt, James J ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NONE

Author keywords

MRI; neuroimaging; olfaction; olfactory function; schizophrenia

Indexed keywords

APOLIPOPROTEIN E4; GUANINE NUCLEOTIDE BINDING PROTEIN;

AMYGDALOID NUCLEUS; ANOREXIA NERVOSA; BIPOLAR DISORDER; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC LINKAGE; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; MAJOR DEPRESSION; MONOZYGOTIC TWINS; NEGATIVE SYNDROME; NEUROANATOMY; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY DISCRIMINATION; OLFACTORY MEMORY; OLFACTORY NERVE DISEASE; ORBITAL CORTEX; PATHOPHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; REVIEW; SCHIZOPHRENIA; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY; THALAMUS;

FEMALE; FRONTAL LOBE; HUMANS; LIMBIC SYSTEM; MALE; OLFACTION DISORDERS; OLFACTORY BULB; OLFACTORY PATHWAYS; SCHIZOPHRENIA; SMELL; TEMPORAL LOBE;

EID: 77956510748     PISSN: 10673229     EISSN: 14657309     Source Type: Journal    
DOI: 10.3109/10673229.2010.511060     Document Type: Review

References (88)

1. Kopala L, Clark C, Hurwitz TA. Olfactory deficits in neuroleptic naïve patients with schizophrenia. Schizophr Res 1993;8:245-250
2. Kopala L, Good K, Martzke J, Hurwitz T. Olfactory deficits in schizophrenia is not a function of task complexity. Schizophr Res 1995;17:195-199
3. Good KP, Martzke JS, Honer WG, Kopala LC. Left nostril identification impairment in a subgroup of male patients with schizophrenia. Schizophr Res 1998;33:35-43.
4. Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL. Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 1999;21:325-340
5. Turetsky BI, Moberg PJ, Owzar K, Johnson SC, Doty RL, Gur RE. Physiologic impairment of olfactory stimulus processing in schizophrenia. Biol Psychiatry 2003;53:403-411
6. Turestsky BI, Moberg PJ, Roalf DR, Arnold SE, Gur RE. Decrements in volume of anterior ventromedial temporal lobe and olfactory dysfunction in schizophrenia. Arch Gen Psychiatry 2003;60:1193-1200
7. Wu J, Buchsbaum MS, Moy K, et al. Olfactory memory in unmedicated schizophrenics. Schizophr Res 1993;9:41-47
8. Rupp CI. Dysfunction in olfactory processing in schizophrenia. Curr Opin Psychiatry 2003;16:181-185
9. Crespo-Facorro B, Kim J, Andreasen ND, et al. Neural mechanisms of anhedonia in schizophrenia: a PET study of response to unpleasant and pleasant odors. JAMA 2001;286: 427-435
10. Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI in schizophrenia. Schizophr Res 2001;49:1-52.
11. Corcoran C, Whitaker A, Coleman E, et al. Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophr Res 2005;80:283-293
12. Malaspina D, Coleman E, Goetz RR, et al. Odor identification, eye tracking and deficit syndrome schizophrenia. Biol Psychiatry 2002;51:809-815
13. Brewer WJ, Pantelis C, Anderson V, et al. Stability of olfactory identification deficits in neuroleptic-naïve patients with first-episode psychosis. Am J Psychiatry 2001;158: 107-115
14. Brewer WJ, Wood SJ, McGorry PD, et al. Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. Am J Psychiatry 2003;160:1790-1794
15. Kopala LC, Good KP, Honer WG. Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophr Res 1994;12: 205-211
16. Rupp CI, Fleischhacker WW, Kemmler G, et al. Various bilateral olfactory deficits in male patients with schizophrenia. Schizophr Bull 2005;31:155-165
17. Atanasova B, Graux J, Hage WE, Hommet C, Camus V, Belzung C. Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev 2008;32: 1315-1325
18. Dade LA, Zatorre RJ, Jones-Gotman M. Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain 2002;125:86-101.
19. Seckinger RA, Goudsmit N, Coleman E, et al. Olfactory identification and WAIS-R performance in deficit and nondeficit schizophrenia. Schizophr Res 2004;69:55-65.
20. Turetsky BI, Kohler CG, Gur RE, Moberg PJ. Olfactory physiological impairment in first-degree relatives of schizophrenia patients. Schizophr Res 2008;102:220-229
21. Malaspina D, Coleman E. Olfaction and social drive in schizophrenia. Arch Gen Psychiatry 2003;60:578-584
22. Kohler CG, Barrett FS, Gur RC, Turetsky BI, Moberg PJ. Association between facial emotion recognition and odor identification in schizophrenia. J Neuropsychiatry Clin Neurosci 2007;19:128-131
23. Good KP, Whitehorn D, Rui Q, Milliken H, Kopala LC. Olfactory identification deficits in first-episode psychosismay predict patients at risk for persistent negative and disorganized or cognitive symptoms. Am J Psychiatry 2006;163:932-933
24. Good KP, Martzke JS, Milliken HI, Honer WG, Kopala LC. Unirhinal olfactory identification deficits in young male patients with schizophrenia and related disorders: association with impaired memory function. Schizophr Res 2002;56:211-223
25. Compton MT, Mack LM, Esterberg ML, et al. Associations between olfactory identification and verbal memory in patients with schizophrenia, first-degree relatives, and non-psychiatric controls. Schizophr Res 2006;86:154-166
26. Brewer WJ, Wood SJ, Pantelis C, Berger GE, Copolov DL, McGorry PD. Olfactory sensitivity through the course of psychosis: relationships to olfactory identification, symptomatology and the schizophrenia odour. Psychiatry Res 2007; 149:97-104.
27. Crespo-Facorro B, Kim JJ, Andreasen NC, O'Leary DS, Bockholt JH, Magnotta V. Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of first-episode patients. Schizophr Res 2000;46:35-43.
28. Gur RE, Turetsky BI, Cowell PE, et al. Temporolimbic volume reductions in schizophrenia. Arch Gen Psychiatry 2000;57:769-775
29. Hudry J, Saoud M, D'Amato T, Dalery J, Royet JP. Ratings of different olfactory judgements in schizophrenia. Chem Senses 2002;27:407-416
30. Kasai K, Shenton ME, Salisbury DF, et al. Differences and similarities in insular and temporal pole MRI gray matter volume abnormalities in first-episode schizophrenia and affective psychosis. Arch Gen Psychiatry 2003;60:1069-1077
31. Gur RE, Cowell PE, Latshaw A, et al. Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Arch Gen Psychiatry 2000;57:761-768
32. Crespo-Facorro B, Kim JJ, Andreasen NC, O'Leary DS, Ymagnotta V. Regional frontal abnormalities in schizophrenia: a quantitative gray matter volume and cortical surface size study. Biol Psychiatry 2008;48:110-119
33. Compton MT, Chien VH. No association between psychometrically-determined schizotypy and olfactory identification ability in first-degree relatives of patients with schizophrenia and non-psychiatric controls. Schizophr Res 2008;100:216-223
34. Moberg PJ, McGue C, Kanes SJ, et al. Phenylthiocarbamide (PTC) perception in patients with schizophrenia and firstdegree family members: relationship to clinical symptomatology and psychophysical olfactory performance. Schizophr Res 2007;90:221-228
35. Butler PD, Silverstein SM, Dakin SC. Visual perception and its impairments in schizophrenia. Biol Psychiatry 2008;64:40-47
36. Hummel T, Damm M, Vent J, et al. Depth of olfactory sulcus and olfactory function. Brain Res 2003;975:85-89
37. Abolmaali ND, Hietschold V, Vogl TJ, Huttenbrink KB, Hummel T. MR evaluation in patients with isolated anosmia since birth or early childhood. Am J Neuroradiol 2002;23:157-164
38. Turetsky BI, Hahn CG, Arnold SE, Moberg PJ. Olfactory receptor neuron dysfunction in schizophrenia. Neuropsychopharmacology 2009;34:767-774
39. Ugur T, Weisbrod M, Franzek E, Pfuller U, Sauer H. Olfactory impairment in monozygotic twins discordant for schizophrenia. Eur Arch Psychiatry Clin Neurosci 2005;255:94-98
40. Kopala LC, Good KP, Morrison K, Bassett AS, Alda M, Honer WG. Impaired olfactory identification in relatives of patients with familial schizophrenia. Am J Psychiatry 2001;158:1286-1290
41. Turetsky BI, Moberg PJ, Arnold SE, Doty RL, Gur RE. Low olfactory bulb volume in first-degree relatives of patients with schizophrenia. Am J Psychiatry 2003;160:703-708
42. Schneider F, Habel U, Reske M, Toni I, Falkai P, Shah NJ. Neural substrates of olfactory processing in schizophrenia patients and their healthy relatives. Psychiatry Res 2007;155:103-112
43. Turetsky BI, Moberg PJ, Youse DM, Doty RL, Arnold SE, Gur RE. Reduced olfactory bulb volume in patients with schizophrenia. Am J Psychiatry 2000;157:828-830
44. Kohler CG, Moberg PJ, Gur RE, O'Conner MJ, Sperling MR, Goty RL. Olfactory dysfunction in schizophrenia and temporal lobe epilepsy. Neuropsychiatry Neuropsychol Behav Neurol 2001;14:83-88
45. Moberg PJ, Arnold SE, Doty RL, et al. Impairment of odor hedonics in men with schizophrenia. Am J Psychiatry 2003;160:1784-1789
46. Rupp CI, Fleischhacker WW, Kemmler G, et al. Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia. Schizophr Res 2005;74:149-161
47. Plailly J, D'Amato T, Saoud M, Royet JP. Left temporolimbic and orbital dysfunction in schizophrenia during odor familiarity and hedonicity judgments. Neuroimage 2006;29:302-313
48. Roalf DR, Turesky BI, Owzar K, et al. Unirhinal olfactory function in schizophrenia patients and first-degree relatives. J Neuropsychiatry Clin Neurosci 2006;18:389-396
49. Moberg PJ, Arnold SE, Doty RL, Gur RE, Basderston CC, Roalf DR. Olfactory functioning in schizophrenia: relationship to clinical, neuropsychological, and volumetric MRI measures. J Clin Exp Neuropsychol 2006;28:1444-1461
50. Moberg PJ, Arnold SE, Roalf DR, Balderson CC, et al. Apolipoprotein E genotype and odor identification in schizophrenia. J Neuropsychiatry Clin Neurosci 2006;18:231-233
51. Plailly J, Howard JD, Gitelman DR, Gottfried JA. Attention to odor modulates thalamocortical connectivity in the human brain. J Neurosci 2008;28:5257-5267
52. Nolte J, Sundsten J. The human brain: an introduction to its functional anatomy. 6th ed. Philadelphia: Mosby, 2008:330-339
53. Hurtwitz T, Kopala L, Clark C, Jones B. Olfactory deficits in schizophrenia. Biol Psychiatry 1988;23:123-128
54. Amsterdam JD, Settle RG, Doty RL, Abelman E, Winokur A. Taste and smell perception in depression. Biol Psychiatry 1987;22:1481-1485
55. Kopala LC, Good K, Goldner EM, Birmingham CL. Olfactory identification ability in anorexia nervosa. J Psychiatry Neurosci 1995;20:283-286
56. Mesholam RI, Moberg PJ, Mahr RN, Doty RL. Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Arch Neurol 1998;55:84-90.
57. Ross DE, Thaker GK, Buchanan RW, et al. Eye tracking disorder in schizophrenia is characterized by specific ocular motor defects and is associated with the deficit syndrome. Biol Psychiatry 1997;42:781-796
58. Ross DE, Thaker GK, Buchanan RW, et al. Association of abnormal smooth pursuit eye movements with the deficit syndrome in schizophrenic patients. Am J Psychiatry 1996;153:1158-1165
59. Feron F, Perry C, McGrath J. Altered adhesions, proliferation and death in neural cultures from adults with schizophrenia. Schizophr Res 1999;40:211-218
60. Eslinger PJ, Damsio AR, Van-Hoesen GM. Olfactory dysfunction in man: anatomical and behavioral aspects. Brain Cogn 1982;1:259-285
61. Prices JL. Olfactory system. The human nervous system. San Diego, CA: Academic, 1990:979-998
62. Carmichael ST, Clugnet MC, Price JL. Central olfactory connections in themacaquemonkey. J Comp Neurol 1994;346:403-434
63. Russchen FT, Amaral DG, Price JL. The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol 1987;256:175-210.
64. Ray JP, Price JL. The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol 1992;323:167-197
65. Potter H, Butters N. An assessment of olfactory deficits in patients with damage to prefrontal cortex. Neuropsychology 1980;18:621-628
66. Gur RE, Turetsky BI, Bilker WB. Reduced gray matter volume in schizophrenia. Arch Gen Psychiatry 1999;56:905-911
67. Clark C, Kopala L, Hurwitz T, Li D. Regional metabolism in microsmic patients with schizophrenia. Can J Psychiatry 1991;36:645-650
68. Malaspina D, Perera GM, Lignelli A, et al. SPECT imaging of odor identification in schizophrenia. Psychiatry Res 1998;82:53-61.
69. Zald DH. The human amygdale and the emotional evaluation of sensory stimuli. Brain Res Rev 2003;41:88-123.
70. Paradiso S, Andreasen NC, Crespo-Facorro B, et al. Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. Am J Psychiatry 2003;160:1775-1783
71. Skosnik PD, Spatz-Glenn L, Park S. Cannabis use is associated with schizotypy and attentional disinhibition. Schizophr Res 2001;48:83-92.
72. Seidman LJ, Talbot NL, Kalinowki AG, McCarley RW, Tsuang MT. Neuropsychological probes of fronto-limbic system dysfunction in schizophrenia: olfactory identification and Wisconsin card sorting performance. Schizophr Res 1992;6:55-65.
73. Kopala L, Clark C. Implications of olfactory agnosia for understanding sex differences in schizophrenia. Schizophr Bull 1990;16:255-261
74. Yousem DM, Geckle RJ, Bilker WB,McKeownDA, Doty RL.MR evaluation of patients with congenital hyposmia or anosmia. Am J Roentgenol 1996;166:439-443
75. Heine O, Galaburda AM. Olfactory asymmetry in the rat brain. Exp Neurol 1986;91:392-398
76. Yousem DM, Geckle RJ, Bilker WB,DotyRL. Olfactory bulb and rat and temporal lobe volumes: normative data across decades. Ann N Y Acad Sci 1998;855:546-555
77. Zatorre RJ, Jones-Gotman M, Evans AC, Meyer E. Functional localization and lateralization of human olfactory cortex. Nature 1992;360:339-340
78. Jones-Gotman M, Zatorre RJ. Odor recognition memory in humans: role of right temporal and orbitofrontal regions. Brain Cogn 1993;22:182-198
79. Hummel T, Pauli E, Schuler P, Kettenmann B, Stefan H, Kobal G. Chemosensory event-related potentials in patients with temporal lobe epilepsy. Epilepsia 1995;36:79-85.
80. Yousem DM, Maldjian JA, Siddiqi F, et al. Gender effects on odor-stimulated functional magnetic resonance imaging. Brain Res 1999;818:480-487
81. Sobel N, Khan RM, Saltman A, Sullivan EV, Gabrieli JD. The world smells different to each nostril. Nature 1999;402: 35.
82. Fulbright RK, Skudlarski P, Lacadie CM, et al. Functional MR imaging of regional brain responses to pleasant and unpleasant odors. Am J Neuroradiol 1998;19:1721.
83. Moberg P, Doty R, Turetsky B, Wylonis T, Acosta T, Gur E. Olfactory functioning in siblings discordant for schizophrenia [Abstract]. Biol Psychiatry 1996;39:571-572
84. Kopala LC, Good KP, Torrey EF, Honer WG. Olfactory function in monozygotic twins discordant for schizophrenia. Am J Psychiatry 1998;155:134-136
85. Cain WS. Bilateral interaction in olfaction. Nature 1977;268:50-52
86. Bromley SM, Doty RL.Odor recognition memory is better under bilateral than unilateral test conditions. Cortex 1995;31:25-40.
87. Hirayasu Y, McCarley RW, Salisbury DF, et al. Planum temporal and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients. Arch Gen Psychiatry 2000;57:692-699
88. Kasai K, Shenton ME, Salisbury DF, et al. Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 2003;60:766-775