Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T12:52:06.011Z Has data issue: false hasContentIssue false
  • English
  • Français

The 5% difference: early sensory processing predicts sarcasm perception in schizophrenia and schizo-affective disorder

Published online by Cambridge University Press:  24 April 2013

J. T. Kantrowitz ,
M. J. Hoptman ,
D. I. Leitman ,
G. Silipo  and
D. C. Javitt
J. T. Kantrowitz*
Affiliation:
Schizophrenia Research Center, Nathan Kline Institute, Orangeburg, NY, USA Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USA
M. J. Hoptman
Affiliation:
Schizophrenia Research Center, Nathan Kline Institute, Orangeburg, NY, USA Department of Psychiatry, New York University, New York, NY, USA
D. I. Leitman
Affiliation:
Department of Neuropsychiatry, University of Pennsylvania, Philadelphia, PA, USA
G. Silipo
Affiliation:
Schizophrenia Research Center, Nathan Kline Institute, Orangeburg, NY, USA
D. C. Javitt
Affiliation:
Schizophrenia Research Center, Nathan Kline Institute, Orangeburg, NY, USA Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USA
*
*Address for correspondence: J. T. Kantrowitz, M.D., Nathan Kline Institute for Psychiatric Research, 140 Old Orangeburg Rd, Orangeburg, NY 10962, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Intact sarcasm perception is a crucial component of social cognition and mentalizing (the ability to understand the mental state of oneself and others). In sarcasm, tone of voice is used to negate the literal meaning of an utterance. In particular, changes in pitch are used to distinguish between sincere and sarcastic utterances. Schizophrenia patients show well-replicated deficits in auditory function and functional connectivity (FC) within and between auditory cortical regions. In this study we investigated the contributions of auditory deficits to sarcasm perception in schizophrenia.

Method

Auditory measures including pitch processing, auditory emotion recognition (AER) and sarcasm detection were obtained from 76 patients with schizophrenia/schizo-affective disorder and 72 controls. Resting-state FC (rsFC) was obtained from a subsample and was analyzed using seeds placed in both auditory cortex and meta-analysis-defined core-mentalizing regions relative to auditory performance.

Results

Patients showed large effect-size deficits across auditory measures. Sarcasm deficits correlated significantly with general functioning and impaired pitch processing both across groups and within the patient group alone. Patients also showed reduced sensitivity to alterations in mean pitch and variability. For patients, sarcasm discrimination correlated exclusively with the level of rsFC within primary auditory regions whereas for controls, correlations were observed exclusively within core-mentalizing regions (the right posterior superior temporal gyrus, anterior superior temporal sulcus and insula, and left posterior medial temporal gyrus).

Conclusions

These findings confirm the contribution of auditory deficits to theory of mind (ToM) impairments in schizophrenia, and demonstrate that FC within auditory, but not core-mentalizing, regions is rate limiting with respect to sarcasm detection in schizophrenia.

Keywords

AuditoryMRIresting statesarcasmschizophreniatheory of mind
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 1 , January 2014 , pp. 25 - 36
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.)

References

Abu-Akel, A, Shamay-Tsoory, S (2011). Neuroanatomical and neurochemical bases of theory of mind. Neuropsychologia 49, 2971–2984.CrossRefGoogle ScholarPubMed
Banse, R, Scherer, K (1996). Acoustic profiles in vocal emotion expression. Journal of Personality and Social Psychology 70, 614–636.CrossRefGoogle ScholarPubMed
Biedermann, F, Frajo-Apor, B, Hofer, A (2012). Theory of mind and its relevance in schizophrenia. Current Opinion in Psychiatry 25, 71–75.CrossRefGoogle ScholarPubMed
Biswal, B, Yetkin, FZ, Haughton, VM, Hyde, JS (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine 34, 537–541.Google Scholar
Biswal, B, Mennes, M, Zuo, XN, Gohel, S, Kelly, C, Smith, S, Beckmann, C, Bucker, R, Colcombe, S, Dogonowski, A-M, Ernst, M, Hyde, JS, Kotter, R, McMahon, K, Maddon, D, Madsen, K, Butler, PD, Hampson, M, Hoptman, MJ, Kiviniemi, V, Li, S-J, Lin, C-P, Lowe, M, Mayberg, H, Peltier, S, Petersen, S, Raichle, M, Rombouts, S, Rypma, B, Schlagger, B, Schmidt, S, Siegle, GJ, Sorg, C, Teng, G-J, Villringer, A, Walter, M, Wang, L-H, Whitfield-Gabrieli, S, Windishchberger, C, Zhang, H-Y, Zang, Y-F, Castellanos, FX, Milham, MP (2010). Toward discovery science of human brain function. Proceedings of the National Academy of Sciences USA 107, 4734–4739.Google Scholar
Boersma, P (2001). Praat, a system for doing phonetics by computer. Glot International 5, 341–345.Google Scholar
Bowie, CR, Leung, WW, Reichenberg, A, McClure, MM, Patterson, TL, Heaton, RK, Harvey, PD (2008). Predicting schizophrenia patients’ real-world behavior with specific neuropsychological and functional capacity measures. Biological Psychiatry 63, 505–511.Google Scholar
Cheang, HS, Pell, MD (2008). The sound of sarcasm. Speech Communication 50, 366–381.CrossRefGoogle Scholar
Cheang, HS, Pell, MD (2009). Acoustic markers of sarcasm in Cantonese and English. Journal of the Acoustical Society of America 126, 1394–1405.Google Scholar
Clark, VP, Coffman, BA, Mayer, AR, Weisend, MP, Lane, TD, Calhoun, VD, Raybourn, EM, Garcia, CM, Wassermann, EM (2012). TDCS guided using fMRI significantly accelerates learning to identify concealed objects. NeuroImage 59, 117–128.CrossRefGoogle ScholarPubMed
Cohen, J (1988). Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Cox, RW (1996). Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162–173.CrossRefGoogle ScholarPubMed
Das, P, Calhoun, V, Malhi, GS (2012 a). Mentalizing in male schizophrenia patients is compromised by virtue of dysfunctional connectivity between task-positive and task-negative networks. Schizophrenia Research 140, 51–58.Google Scholar
Das, P, Lagopoulos, J, Coulston, CM, Henderson, AF, Malhi, GS (2012 b). Mentalizing impairment in schizophrenia: a functional MRI study. Schizophrenia Research 134, 158–164.CrossRefGoogle ScholarPubMed
Demirtas-Tatlidede, A, Vahabzadeh-Hagh, AM, Pascual-Leone, A (2013). Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders? Neuropharmacology 64, 566–578.Google Scholar
Fett, AK, Viechtbauer, W, Dominguez, MD, Penn, DL, van Os, J, Krabbendam, L (2011). The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neuroscience and Biobehavioral Reviews 35, 573–588.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1994). Structured Clinical Interview for Axis I DSM-IV Disorders – Patient Edition (SCID-I/P). Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Fisher, M, Holland, C, Merzenich, MM, Vinogradov, S (2009). Using neuroplasticity-based auditory training to improve verbal memory in schizophrenia. American Journal of Psychiatry 166, 805–811.Google Scholar
Fong, CT (2006). The effects of emotional ambivalence on creativity. Academy of Management Journal 49, 1016–1030.CrossRefGoogle Scholar
Friston, KJ (1994). Functional and effective connectivity in neuroimaging: a synthesis. Human Brain Mapping 2, 56–78.CrossRefGoogle Scholar
Gibbs, RW Jr. (1986). On the psycholinguistics of sarcasm. Journal of Experimental Psychology: General 115, 3–15.Google Scholar
Gibbs, RW Jr. (2000). Irony in talk among friends. Metaphor and Symbol 15, 5–27.Google Scholar
Gold, R, Butler, PD, Revheim, N, Leitman, DI, Hansen, JA, Gur, RC, Kantrowitz, JT, Laukka, P, Juslin, PN, Silipo, GS, Javitt, DC (2012). Auditory emotion recognition impairments in schizophrenia: relationship to acoustic features and cognition. American Journal of Psychiatry 169, 424–432.Google Scholar
Green, M, Leitman, D (2008). Social cognition in schizophrenia. Schizophrenia Bulletin 34, 670–672.CrossRefGoogle ScholarPubMed
Hagmann, P, Cammoun, L, Gigandet, X, Meuli, R, Honey, CJ, Wedeen, VJ, Sporns, O (2008). Mapping the structural core of human cerebral cortex. PLoS Biol 6, e159.Google Scholar
Hall, RC (1995). Global assessment of functioning. A modified scale. Psychosomatics 36, 267–275.Google Scholar
Hoptman, MJ, Zuo, XN, Butler, PD, Javitt, DC, D'Angelo, D, Mauro, CJ, Milham, MP (2010). Amplitude of low-frequency oscillations in schizophrenia: a resting state fMRI study. Schizophrenia Research 117, 13–20.CrossRefGoogle ScholarPubMed
Jorgenson, J (1996). The functions of sarcastic irony in speech. Journal of Pragmatics 26, 613–634.Google Scholar
Juslin, PN, Laukka, P (2001). Impact of intended emotion intensity on cue utilization and decoding accuracy in vocal expression of emotion. Emotion 1, 381–412.Google Scholar
Kantrowitz, JT, Leitman, DI, Lehrfeld, JM, Laukka, P, Juslin, PN, Butler, PD, Silipo, G, Javitt, DC (2013). Reduction in tonal discriminations predicts receptive emotion processing deficits in schizophrenia and schizoaffective disorder. Schizophrenia Bulletin 39, 86–93.CrossRefGoogle ScholarPubMed
Kantrowitz, JT, Revheim, N, Pasternak, R, Silipo, G, Javitt, DC (2009). It's all in the cards: effect of stimulus manipulation on Wisconsin Card Sorting Test performance in schizophrenia. Psychiatry Research 168, 198–204.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.Google Scholar
Kelly, AMC, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2008). Competition between functional brain networks mediates behavioral variability. NeuroImage 39, 527–537.Google Scholar
Kern, RS, Gold, JM, Dickinson, D, Green, MF, Nuechterlein, KH, Baade, LE, Keefe, RS, Mesholam-Gately, RI, Seidman, LJ, Lee, C, Sugar, CA, Marder, SR (2011). The MCCB impairment profile for schizophrenia outpatients: results from the MATRICS psychometric and standardization study. Schizophrenia Research 126, 124–131.Google Scholar
Kern, RS, Green, MF, Fiske, AP, Kee, KS, Lee, J, Sergi, MJ, Horan, WP, Subotnik, KL, Sugar, CA, Nuechterlein, KH (2009). Theory of mind deficits for processing counterfactual information in persons with chronic schizophrenia. Psychological Medicine 39, 645–654.CrossRefGoogle ScholarPubMed
Kipps, CM, Nestor, PJ, Acosta-Cabronero, J, Arnold, R, Hodges, JR (2009). Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. Brain 132, 592–603.Google Scholar
Leitman, DI, Hoptman, MJ, Foxe, JJ, Saccente, E, Wylie, GR, Nierenberg, J, Jalbrzikowski, M, Lim, KO, Javitt, DC (2007). The neural substrates of impaired prosodic detection in schizophrenia and its sensorial antecedents. American Journal of Psychiatry 164, 474–482.Google Scholar
Leitman, DI, Laukka, P, Juslin, PN, Saccente, E, Butler, P, Javitt, DC (2010). Getting the cue: sensory contributions to auditory emotion recognition impairments in schizophrenia. Schizophrenia Bulletin 36, 545–556.Google Scholar
Leitman, DI, Wolf, DH, Laukka, P, Ragland, JD, Valdez, JN, Turetsky, BI, Gur, RE, Gur, RC (2011). Not pitch perfect: sensory contributions to affective communication impairment in schizophrenia. Biological Psychiatry 70, 611–618.Google Scholar
Leitman, DI, Ziwich, R, Pasternak, R, Javitt, DC (2006). Theory of Mind (ToM) and counterfactuality deficits in schizophrenia: misperception or misinterpretation? Psychological Medicine 36, 1075–1083.Google Scholar
Li, HJ, Chan, RC, Gong, QY, Liu, Y, Liu, SM, Shum, D, Ma, ZL (2012). Facial emotion processing in patients with schizophrenia and their non-psychotic siblings: a functional magnetic resonance imaging study. Schizophrenia Research 134, 143–150.Google Scholar
Loughead, JW, Luborsky, L, Weingarten, CP, Krause, ED, German, RE, Kirk, D, Gur, RC (2010). Brain activation during autobiographical relationship episode narratives: a core conflictual relationship theme approach. Psychotherapy Research 20, 321–336.Google Scholar
Mancuso, F, Horan, WP, Kern, RS, Green, MF (2011). Social cognition in psychosis: multidimensional structure, clinical correlates, and relationship with functional outcome. Schizophrenia Research 125, 143–151.Google Scholar
Mar, RA (2011). The neural bases of social cognition and story comprehension. Annual Review of Psychology 62, 103–134.Google Scholar
Margulies, DS, Kelly, AM, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37, 579–588.Google Scholar
Materna, S, Dicke, PW, Thier, P (2008). The posterior superior temporal sulcus is involved in social communication not specific for the eyes. Neuropsychologia 46, 2759–2765.Google Scholar
Miron-Spektor, E, Efrat-Treister, D, Rafaeli, A, Schwarz-Cohen, O (2011). Others’ anger makes people work harder not smarter: the effect of observing anger and sarcasm on creative and analytic thinking. Journal of Applied Psychology 96, 1065–1075.CrossRefGoogle Scholar
Mitchell, RL, Ross, ED (2008). fMRI evidence for the effect of verbal complexity on lateralisation of the neural response associated with decoding prosodic emotion. Neuropsychologia 46, 2880–2887.Google Scholar
Norton, DJ, McBain, RK, Ongur, D, Chen, Y (2011). Perceptual training strongly improves visual motion perception in schizophrenia. Brain and Cognition 77, 248–256.Google Scholar
Orbelo, DM, Grim, MA, Talbott, RE, Ross, ED (2005). Impaired comprehension of affective prosody in elderly subjects is not predicted by age-related hearing loss or age-related cognitive decline. Journal of Geriatric Psychiatry and Neurology 18, 25–32.Google Scholar
Pedersen, A, Koelkebeck, K, Brandt, M, Wee, M, Kueppers, KA, Kugel, H, Kohl, W, Bauer, J, Ohrmann, P (2012). Theory of mind in patients with schizophrenia: is mentalizing delayed? Schizophrenia Research 137, 224–229.Google Scholar
Power, JD, Barnes, KA, Snyder, AZ, Schlaggar, BL, Petersen, SE (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59, 2142–2154.CrossRefGoogle ScholarPubMed
Revheim, N, Medalia, A (2004). The independent living scales as a measure of functional outcome for schizophrenia. Psychiatric Services 55, 1052–1054.Google Scholar
Rockwell, P (2000). Actors’, partners’, and observers’ perceptions of sarcasm. Perceptual and Motor Skills 91, 665–668.Google Scholar
Rockwell, P (2007). Vocal features of conversational sarcasm: a comparison of methods. Journal of Psycholinguistic Research 36, 361–369.CrossRefGoogle ScholarPubMed
Smith, EE, White, HL (1965). Wit, creativity and sarcasm. Journal of Applied Psychology 49, 131–134.Google Scholar
Sparks, A, McDonald, S, Lino, B, O'Donnell, M, Green, MJ (2010). Social cognition, empathy and functional outcome in schizophrenia. Schizophrenia Research 122, 172–178.Google Scholar
Turner, JA, Chen, H, Mathalon, DH, Allen, EA, Mayer, AR, Abbott, CC, Calhoun, VD, Bustillo, J (2012). Reliability of the amplitude of low-frequency fluctuations in resting state fMRI in chronic schizophrenia. Psychiatry Research 201, 253–255.Google Scholar
Uchiyama, H, Seki, A, Kageyama, H, Saito, DN, Koeda, T, Ohno, K, Sadato, N (2006). Neural substrates of sarcasm: a functional magnetic-resonance imaging study. Brain Research 1124, 100–110.Google Scholar
Uchiyama, HT, Saito, DN, Tanabe, HC, Harada, T, Seki, A, Ohno, K, Koeda, T, Sadato, N (2012). Distinction between the literal and intended meanings of sentences: a functional magnetic resonance imaging study of metaphor and sarcasm. Cortex 48, 563–583.Google Scholar
Vollm, BA, Taylor, AN, Richardson, P, Corcoran, R, Stirling, J, McKie, S, Deakin, JF, Elliott, R (2006). Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage 29, 90–98.Google Scholar
Wechsler, DA (1997). Wechsler Adult Intelligence Scale-III. Psychological Corporation: New York.Google Scholar
Winner, E, Brownell, H, Happe, F, Blum, A, Pincus, D (1998). Distinguishing lies from jokes: theory of mind deficits and discourse interpretation in right hemisphere brain-damaged patients. Brain and Language 62, 89–108.Google Scholar
Worsley, KJ (2001). Statistical analysis of activation images. In Functional MRI: An Introduction to Methods (ed. Jezzard, P., Matthew, P. M. and Smith, S. M.), pp. 251–270. Oxford University Press: Oxford, UK.Google Scholar
Supplementary material: File

Kantrowitz Supplementary Material

Tables S1-S5

Download Kantrowitz Supplementary Material(File)
File 122.4 KB