Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-28T05:26:21.778Z Has data issue: false hasContentIssue false

Relationship between olfactory function and social cognition in euthymic bipolar patients

Published online by Cambridge University Press:  12 June 2013

Guillermo Lahera*
Affiliation:
Department of Medicine and Medical Specialties (Psychiatry), University of Alcala, Madrid, Spain
Salvador Ruiz-Murugarren
Affiliation:
Department of Psychiatry, Príncipe de Asturias University Hospital, Alcala, Madrid, Spain
Alberto Fernández-Liria
Affiliation:
Department of Medicine and Medical Specialties (Psychiatry), University of Alcala, Madrid, Spain Department of Psychiatry, Príncipe de Asturias University Hospital, Alcala, Madrid, Spain
Jerónimo Saiz-Ruiz
Affiliation:
Department of Medicine and Medical Specialties (Psychiatry), University of Alcala, Madrid, Spain Department of Psychiatry, Ramón y Cajal University Hospital, Mental Health National Net IRYCIS: CIBERSAM, Madrid, Spain
Benjamin E. Buck
Affiliation:
Department of Psychology, University of North Carolina-Chapel Hill, NC, USA
David L. Penn
Affiliation:
Department of Psychology, University of North Carolina-Chapel Hill, NC, USA
*
*Address for correspondence: Guillermo Lahera, Lope de Rueda 3, 28009 Madrid, Spain. (Email guillermo.lahera@uah.es)

Abstract

Objective/Introduction

There is a close functional and neuroanatomical relationship between olfactory ability and emotional processing. The present study seeks to explore the association between olfactory ability and social cognition, especially facial emotion perception, in euthymic bipolar patients.

Methods

Thirty-nine euthymic outpatients meeting DSM-IV-TR criteria for bipolar disorder and 40 healthy volunteers matched on socio-demographic criteria were recruited. Both groups were assessed at one time point with the University of Pennsylvania Smell Identification Test (UPSIT), the Emotion Recognition Test, and The Faux Pas Recognition Test, as well as measures of general cognition and functioning.

Results

The bipolar patients showed a significant impairment in olfactory identification (UPSIT) and social cognition measures compared to healthy controls. Analyses revealed significant relationships between olfactory identification and facial emotion recognition, theory of mind, general cognition, and a trend-level relationship with functioning. Controlling for age and cigarettes smoked, relationships remained significant between olfactory function and facial emotion recognition.

Conclusion

There is a deficit of olfactory identification in euthymic patients with bipolar disorder that is correlated with a deficit in both verbal and non-verbal measures of social cognition.

Type
Original Research
Copyright
Copyright © Cambridge University Press 2013 

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.)

Footnotes

The authors wish to thank the Foundation for Biomedical Research (Príncipe de Asturias University Hospital) for the grant support.

References

1. Martzke, JS, Kopala, LC, Good, KP. Olfactory dysfunction in neuropsychiatric disorders: review and methodological considerations. Biol Psychiatry. 1997; 42(8): 721732.Google Scholar
2. Atanasova, B, Graux, J, El Hage, W, etal. Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev. 2008; 32: 13151325.Google Scholar
3. Kivity, S, Ortega-Hernandez, OD, Shoenfeld, Y. Olfaction—a window to the mind. Isr Med Assoc J. 2009; 11: 238243.Google ScholarPubMed
4. Kopala, L, Clark, C, Hurwitz, TA. Olfactory deficits in neuroleptic naive patients with schizophrenia. Schizophr Res. 1993; 8: 245250.Google Scholar
5. Moberg, PJ, Agrin, R, Gur, RE, etal. Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology. 1999; 21: 325341.CrossRefGoogle ScholarPubMed
6. Stedman, TJ, Clair, AL. Neuropsychological, neurological and symptom correlates of impaired olfactory identification in schizophrenia. Schizophr Res. 1998; 32: 2330.Google Scholar
7. Moberg, PJ, Arnold, SE, Doty, RL, etal. Impairment of odor hedonics in men with schizophrenia. Am J Psychiatry. 2003; 160: 17841789.CrossRefGoogle ScholarPubMed
8. Postolache, TT, Doty, RL, Wehr, TA, etal. Monorhinal odor identification and depression scores in patients with seasonal affective disorder. J Affect Disord. 1999; 56(1): 2735.CrossRefGoogle ScholarPubMed
9. Postolache, TT, Wehr, TA, Doty, RL, etal. Patients with seasonal affective disorder have lower odor detection thresholds than control subjects. Arch Gen Psychiatry. 2002; 59(12): 11191122.Google Scholar
10. Pause, BM, Miranda, A, Göder, R, Aldenhoff, JB, Ferstl, R. Reduced olfactory performance in patients with major depression. J Psychiatr Res. 2001; 35(5): 271277.CrossRefGoogle ScholarPubMed
11. Lombion-Pouthier, S, Vandel, P, Nezelof, S, Haffen, E, Millot, JL. Odor perception in patients with mood disorders. J Affect Disord. 2006; 90(2–3): 187191.Google Scholar
12. Hurwitz, TA, Kopala, L, Clark, C, Jones, B. Olfactory deficits in schizophrenia. Biol Psychiatry. 1988; 23: 123128.CrossRefGoogle ScholarPubMed
13. Amsterdam, JD, Settle, RG, Doty, RL, Abelman, E. Taste and smell perception in depression. Biol Psychiatry. 1987; 22: 14811485.Google Scholar
14. Warner, MD, Peabody, CA, Csernansky, JG. Olfactory functioning in schizophrenia and depression. Biol Psychiatry. 1990; 27: 457458.Google Scholar
15. Serby, M, Larson, P, Kalkstein, D. Olfactory senses in psychoses. Biol Psychiatry. 1990; 28: 829830.Google Scholar
16. Solomon, GS, Petrie, WM, Hart, JR, Brackin, HB. Olfactory dysfunction discriminates Alzheimer's dementia from major depression. J Neuropsychiatry Clin Neurosci. 1998; 10: 6467.Google Scholar
17. Swiecicki, L, Zatorski, P, Bzinkowska, D, etal. Gustatory and olfactory function in patients with unipolar and bipolar depression. Prog Neuropsychopharmacol Biol Psychiatry. 2009; 33: 827834.Google Scholar
18. Brewer, WJ, Pantelis, C, Anderson, V, etal. Stability of olfactory identification deficits in neuroleptic-naïve patients with first-episode psychosis. Am J Psychiatry. 2001; 158: 107115.Google Scholar
19. Cumming, AG, Matthews, NL, Park, S. Olfactory identification and preference in bipolar disorder and schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2011; 261(4): 251259.Google Scholar
20. Hardy, C, Rosedale, M, Messinger, JW, etal. Olfactory acuity is associated with mood and function in a pilot study of stable bipolar disorder patients. Bipolar Disord. 2012; 14(1): 109117.Google Scholar
21. Millot, JL, Brand, G. Effects of pleasant and unpleasant ambient odors on human voice pitch. Neurosci Lett. 2001; 297: 6163.CrossRefGoogle ScholarPubMed
22. Miltner, W, Matjak, C, Braun, H, Diekmann, H, Brody, S. Emotional qualities of odors and their influence on the startle reflex in humans. Psychophysiology. 1994; 31: 107110.Google Scholar
23. Ludvigson, HW, Rottman, TR. Effects of ambient odors of lavender and cloves on cognition, memory, affect and mood. Chem Senses. 1989; 14: 525536.Google Scholar
24. Pitkänen, A, Pikkarainen, M, Nurminen, N, Ylinen, A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat: a review. Ann N Y Acad Sci. 2000; 911: 369391.CrossRefGoogle ScholarPubMed
25. Rolls, ET, Kringelbach, ML, de Araujo, IE. Different representations of pleasant and unpleasant odours in the human brain. Eur J Neurosci. 2003; 189: 695703.Google Scholar
26. Royet, JP, Hudry, J, Zald, DH, etal. Functional neuroanatomy of different olfactory judgments. Neuroimage. 2001; 13(3): 506519.Google Scholar
27. Savic, I. Processing of odorous signals in humans. Brain Res Bull. 2001; 54: 307312.Google Scholar
28. Penn, DL, Spaulding, W, Reed, D, etal. Cognition and social functioning in schizophrenia. Psychiatry. 1997; 60(4): 281291.Google Scholar
29. Baron-Cohen, S, Leslie, AM, Frith, U. Does the autistic child have a “theory of mind”? Cognition. 1985: 3746.Google Scholar
30. Kerr, N, Dunbar, RI, Bentall, RP. Theory of mind deficits in bipolar affective disorder. J Affect Disord. 2003; 73: 253259.Google Scholar
31. Lahera, G, Montes, JM, Benito, A, etal. Theory of mind deficit in bipolar disorder: is it related to a previous history of psychotic symptoms? Psychiatry Res. 2008; 161: 309317.Google Scholar
32. Montag, C, Ehrlich, A, Neuhaus, K, etal. Theory of mind impairments in euthymic bipolar patients. J Affect Disord. 2010; 123: 264269.Google Scholar
33. Martino, DJ, Strejilevich, SA, Fassi, G, Marengo, E, Igoa, A. Theory of mind and facial emotion recognition in euthymic bipolar I and bipolar II disorders. Psychiatry Res. 2011; 189(3): 379384.Google Scholar
34. Lahera, G, Ruiz-Murugarren, S, Iglesias, P, etal. Social cognition and global functioning in bipolar disorder. J Nerv Ment Dis. 2012; 200(2): 135141.Google Scholar
35. American Psychiatric Association. The Diagnostic and Statistical Manual of Mental Disorders, 4th ed, text rev. Washington, DC: American Psychiatric Association; 1994.Google Scholar
36. Doty, RL, Shaman, P, Dann, M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav. 1984; 32(3): 489502.Google Scholar
37. Baron-Cohen, S, Wheelwright, S, Jolliffe, T. Is there a “language of the eyes”? Evidence from normal adults, and adults with autism or Asperger syndrome. Visual Cognition. 1997; 4: 311331.Google Scholar
38. Stone, VE, Baron-Cohen, S, Knight, RT. Frontal lobe contributions to theory of mind. J Cogn Neurosci. 1998; 10(5): 640656.Google Scholar
39. Gregory, C, Lough, S, Stone, V, etal. Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer's disease: theoretical and practical implications. Brain. 2002; 125(Pt 4): 752764.Google Scholar
40. Asarnow, RF, Nuechterlein, KH, Marder, SR. Span of apprehension performance, neuropsychological functioning, and indices of psychosis-proneness. J Nerv Ment Dis. 1983; 171(11): 662669.Google Scholar
41. Spaulding, W, Garbin, C, Dras, S. Cognitive abnormalities in schizophrenic patients and schizotypal college students. J Nerv Ment Dis. 1989; 177: 717728.Google Scholar
42. Gurpegui, M, Alvarez, E, Bousoño, M, Ciudad, A, Carlos Gómez, J, Olivares, JM, Bousoño, M. Effect of olanzapine or risperidone treatment on some cognitive functions in a one-year follow-up of schizophrenia outpatients with prominent negative symptoms. Eur Neuropsychopharmacol. 2007; 17(11): 725734.Google Scholar
43. Heaton, RK. Wisconsin Card Sorting Test: Manual. Odessa, FL: Neuropsychological Assessment Resources; 1981.Google Scholar
44. Rosa, AR, Sánchez-Moreno, J, Martínez-Aran, A, etal. Validity and reliability of the Functioning Assessment Short Test (FAST) in bipolar disorder. Clin Pract Epidemiol Ment Health. 2007; 3: 5.Google Scholar
45. Kaneda, H, Maeshima, K, Goto, N, etal. Decline in taste and odor discrimination abilities with age, and relationship between gustation and olfaction. Chem Senses. 2000; 25(3): 331337.Google Scholar
46. Green, MF. Cognitive impairment and functional outcome in schizophrenia and bipolar disorder. J Clin Psychiatry. 2006; 67(Suppl 9): 38.CrossRefGoogle ScholarPubMed
47. Diaz, FJ, James, D, Botts, S, etal. Tobacco smoking behaviors in bipolar disorder: a comparison of the general population, schizophrenia, and major depression. Bipolar Disord. 2009; 11(2): 154165.CrossRefGoogle ScholarPubMed
48. Frye, RE, Schwartz, BS, Doty, RL. Dose-related effects of cigarette smoking on olfactory function. JAMA. 1990; 263(9): 12331236.Google Scholar
49. 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(2): 128132.Google Scholar
50. Suzuki, Y, Critchley, HD, Rowe, A, Howlin, P, Murphy, DGM. Impaired olfactory identification in Asperger's syndrome. J Neuropsychiatry Clin Neurosci. 2003; 15(1): 105107.Google Scholar
51. Bennetto, L, Kuschner, ES, Hyman, SL. Olfaction and taste processing in autism. Biol Psychiatry. 2007; 62(9): 10151021.Google Scholar
52. Malaspina, D, Corcoran, C, Goudsmit, N. The impact of olfaction on human social functioning. In: Brewer W, Castle D, Pantelis C, eds. Olfaction and the Brain. Cambridge, UK: Cambridge University Press; 2006: 121143.Google Scholar
53. Van Toller, S. Emotion and the brain. In: Van Toller S, Dodd GH, eds. Perfumery: The Psychology and Biology of Fragrance. London: Chapman and Hall; 1988: 1946.Google Scholar
54. Zald, DH, Pardo, JV. Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci U S A. 1997; 94: 41194124.Google Scholar
55. Rahayel, S, Frasnelli, J, Joubert, S. The effect of Alzheimer's disease and Parkinson's disease on olfaction: a meta-analysis. Behav Brain Res. 2012; 231(1): 6074.CrossRefGoogle ScholarPubMed
56. Haehner, A, Hummel, T, Reichmann, H. Olfactory dysfunction as a diagnostic marker for Parkinson's disease. Expert Rev Neurother. 2009; 9(12): 17731779.Google Scholar
57. Rupp, CI. Dysfunctions in olfactory processing in schizophrenia. Curr Opin Psychiatry. 2003; 16: 181185.Google Scholar
58. Doty, RL, Smith, R, McKeown, DA, Raj, J. Tests of human olfactory function: principal components analysis suggests that most measure a common source of variance. Percept Psychophys. 1994; 56(6): 701707.Google Scholar