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Sensory-based and higher-order operations contribute to abnormal emotional prosody processing in schizophrenia: an electrophysiological investigation

Published online by Cambridge University Press:  10 July 2012

A. P. Pinheiro ,
E. del Re ,
J. Mezin ,
P. G. Nestor ,
A. Rauber ,
R. W. McCarley ,
Ó. F. Gonçalves  and
M. A. Niznikiewicz
A. P. Pinheiro
Affiliation:
Neuropsychophysiology Laboratory, CiPsi, School of Psychology, University of Minho, Braga, Portugal Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA
E. del Re
Affiliation:
Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA
J. Mezin
Affiliation:
Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA
P. G. Nestor
Affiliation:
Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA University of Massachusetts, Boston, MA, USA
A. Rauber
Affiliation:
Phonetics Laboratory, Catholic University of Pelotas, Pelotas, Brazil
R. W. McCarley
Affiliation:
Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA
Ó. F. Gonçalves
Affiliation:
Neuropsychophysiology Laboratory, CiPsi, School of Psychology, University of Minho, Braga, Portugal
M. A. Niznikiewicz*
Affiliation:
Clinical Neuroscience Division, Laboratory of Neuroscience, Department of Psychiatry, Boston VA Healthcare System, Brockton Division and Harvard Medical School, Boston, MA, USA
*
*Address for correspondence: M. Niznikiewicz, Ph.D., Department of Psychiatry-116A, Boston VA Healthcare System, 940 Belmont Street, Brockton, MA 02301, USA. (Email: margaret_niznikiewicz@hms.harvard.edu)
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Abstract

Background

Schizophrenia is characterized by deficits in emotional prosody (EP) perception. However, it is not clear which stages of processing prosody are abnormal and whether the presence of semantic content contributes to the abnormality. This study aimed to examine event-related potential (ERP) correlates of EP processing in 15 chronic schizophrenia individuals and 15 healthy controls.

Method

A total of 114 sentences with neutral semantic content [sentences with semantic content (SSC) condition] were generated by a female speaker (38 with happy, 38 with angry, and 38 with neutral intonation). The same sentences were synthesized and presented in the ‘pure prosody’ sentences (PPS) condition where semantic content was unintelligible.

Results

Group differences were observed for N100 and P200 amplitude: patients were characterized by more negative N100 for SSC, and more positive P200 for angry and happy SSC and happy PPS. Correlations were found between delusions and P200 amplitude for happy SSC and PPS. Higher error rates in the recognition of EP were also observed in schizophrenia: higher error rates in neutral SSC were associated with reduced N100, and higher error rates in angry SSC were associated with reduced P200.

Conclusions

These results indicate that abnormalities in prosody processing occur at the three stages of EP processing, and are enhanced in SSC. Correlations between P200 amplitude for happy prosody and delusions suggest a role that abnormalities in the processing of emotionally salient acoustic cues may play in schizophrenia symptomatology. Correlations between ERP and behavioral data point to a relationship between early sensory abnormalities and prosody recognition in schizophrenia.

Keywords

Delusionsevent-related potentialslanguageN100P200psychopathology
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 3 , March 2013 , pp. 603 - 618
Creative Commons
This work is of the U.S. Government and is not subject to copyright protection in the United States
Copyright
Copyright © Cambridge University Press 2012

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References

American Electroencephalographic Society (1991). Guidelines for standard electrode position nomenclature. Journal of Clinical Neurophysiology 8, 200–202.CrossRefGoogle Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, revised. APA: Washington, DC.Google Scholar
Baltaxe, CA, Simmons, JQ III (1995). Speech and language disorders in children and adolescents with schizophrenia. Schizophrenia Bulletin 21, 677–692.CrossRefGoogle ScholarPubMed
Banse, R, Scherer, KR (1996). Acoustic profiles in vocal emotion expression. Journal of Personality and Social Psychology 70, 614–636.CrossRefGoogle ScholarPubMed
Bozikas, V, Kosmidis, M, Anezoulaki, D, Giannakou, M, Andreou, C, Karavatos, A (2006). Impaired perception of affective prosody in schizophrenia. Journal of Neuropsychiatry and Clinical Neurosciences 18, 81–85.CrossRefGoogle ScholarPubMed
Brekke, J, Kay, DD, Lee, KS, Green, MF (2005). Biosocial pathways to functional outcome in schizophrenia. Schizophrenia Research 80, 213–225.CrossRefGoogle ScholarPubMed
Buchanan, TW, Lutz, K, Mirzazade, S, Specht, K, Shah, NJ, Zilles, K, Jancke, L (2000). Recognition of emotional prosody and verbal components of spoken language: an fMRI study. Cognitive Brain Research 9, 227–238.CrossRefGoogle ScholarPubMed
Chandrasekaran, B, Krishnan, A, Gandour, JT (2009). Sensory processing of linguistic pitch as reflected by the mismatch negativity. Ear and Hearing 30, 552–558.CrossRefGoogle ScholarPubMed
Connolly, JF (1993). The influence of stimulus intensity, contralateral masking and handedness on the temporal N1 and the T complex components of the auditory N1 wave. Electroencephalography and Clinical Neurophysiology 86, 58–68.CrossRefGoogle Scholar
Crowley, KE, Colrain, IM (2004). A review of the evidence for P2 being an independent component process: age, sleep and modality. Clinical Neurophysiology 115, 732–744.CrossRefGoogle ScholarPubMed
Diekhof, EK, Biedermann, F, Ruebsamen, R, Gruber, O (2009). Top-down and bottom-up modulation of brain structures involved in auditory discrimination. Brain Research 1297, 118–123.CrossRefGoogle ScholarPubMed
Dutoit, T, Pagel, V, Pierret, N, Bataille, F, Van Der Vreken, O (1996). The MBROLA Project: towards a set of high-quality speech synthesizers free of use for non-commercial purposes. Proceedings of ICSLP '96 3, 1393–1396.Google Scholar
Edwards, J, Pattison, PE, Jackson, HJ, Wales, RJ (2001). Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophrenia Research 48, 235–253.CrossRefGoogle ScholarPubMed
Ethofer, T, Anders, S, Erb, M, Herbert, C, Wiethoff, S, Kissler, J, Grodd, W, Wildgruber, D (2006). Cerebral pathways in processing of affective prosody: a dynamic causal modeling study. Neuroimage 30, 580–587.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1995). Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II, version 2.0). Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV Axis I Diagnosis-Patient Edition (SCID-I/P, version 2.0). Biometric Research Department, New York State Psychiatric Institute: New York.Google Scholar
Forces, RB, Venables, NC, Sponheim, SR (2008). An auditory processing abnormality specific to liability for schizophrenia. Schizophrenia Research 103, 298–310.CrossRefGoogle Scholar
Gandour, J, Wong, D, Dzemidzic, M, Lowe, M, Tong, Y, Li, X (2003). A cross-linguistic fMRI study of perception of intonation and emotion in Chinese. Human Brain Mapping 18, 149–157.CrossRefGoogle ScholarPubMed
Garety, PA, Kuipers, E, Fowler, D, Freeman, D, Bebbington, PE (2001). A cognitive model of the positive symptoms of psychosis. Psychological Medicine 31, 189–195.CrossRefGoogle ScholarPubMed
Gonsalvez, CJ, Barry, RJ, Rushby, JA, Polich, J (2007). Target-to-target interval, intensity, and P300 from an auditory single-stimulus task. Psychophysiology 44, 245–250.CrossRefGoogle ScholarPubMed
Grandjean, D, Sander, D, Pourtois, G, Schwartz, S, Seghier, ML, Scherer, KR, Vuilleumier, P (2005). The voices of wrath: brain responses to angry prosody in meaningless speech. Nature Neuroscience 8, 145–146.CrossRefGoogle ScholarPubMed
Green, MF, Kern, RS, Braff, DL, Mintz, J (2000). Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the “right stuff”? Schizophrenia Bulletin 26, 119–136.CrossRefGoogle ScholarPubMed
Green, MJ, Williams, LM, Davidson, D (2003). Visual scanpaths to threat-related faces in deluded schizophrenia. Psychiatry Research 3, 271–285.CrossRefGoogle Scholar
Hart, HC, Hall, DA, Palmer, AR (2003). The sound-level-dependent growth in the extent of fMRI activation in Heschl's gyrus is different for low- and high-frequency tones. Hearing Research 179, 104–112.CrossRefGoogle ScholarPubMed
Haskins, B, Shutty, MS, Kellogg, E (1995). Affect processing in chronically psychotic patients: development of a reliable assessment tool. Schizophrenia Research 15, 291–297.CrossRefGoogle ScholarPubMed
Hillyard, SA, Hink, RF, Schwent, VL, Picton, TW (1973). Electrical signs of selective attention in the human brain. Science 182, 177–180.CrossRefGoogle ScholarPubMed
Hoekert, M, Kahn, RS, Pijnenborg, M, Aleman, A (2007). Impaired recognition and expression of emotional prosody in schizophrenia: review and meta-analysis. Schizophrenia Research 96, 135–145.CrossRefGoogle ScholarPubMed
Hollingshead, AB (1965). Two-Factor Index of Social Position. Yale Station: New Haven, CT.Google Scholar
Holt, DJ, Titone, D, Long, LS, Goff, DC, Cather, C, Rauch, SL, Judge, A, Kuperberg, GR (2006). The misattribution of salience in delusional patients with schizophrenia. Schizophrenia Research 83, 247–256.CrossRefGoogle ScholarPubMed
Kang, JI, Kim, J, Seok, J, Chun, JW, Lee, S, Park, H (2009). Abnormal brain response during the auditory emotional processing in schizophrenic patients with chronic auditory hallucinations. Schizophrenia Research 107, 83–91.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The Positive and Negative Syndrome Scale (PANSS). Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Kerr, SL, Neale, JM (1993). Emotion perception in schizophrenia: specific deficit or further evidence of generalized poor performance? Journal of Abnormal Psychology 102, 312–318.CrossRefGoogle ScholarPubMed
Kotz, SA, Meyer, M, Alter, K, Besson, M, von Cramon, DY, Friederici, AD (2003). On the lateralization of emotional prosody: an event-related functional MR investigation. Brain and Language 86, 366–376.CrossRefGoogle ScholarPubMed
Kotz, SA, Paulmann, S (2007). When emotional prosody and semantics dance cheek to cheek: ERP evidence. Brain Research 1151, 107–118.CrossRefGoogle ScholarPubMed
Krishnan, RR, Keefe, R, Kraus, M (2009). Schizophrenia is a disorder of higher order hierarchical processing. Medical Hypotheses 6, 740–744.CrossRefGoogle Scholar
Kucharska-Pietura, K, David, A, Masiak, K, Phillips, M (2005). Perception of facial and vocal affect by people with schizophrenia in early and late stages of illness. British Journal of Psychiatry 187, 523–528.CrossRefGoogle ScholarPubMed
Kumar, S, Sedley, W, Nourski, KV, Kawasaki, H, Oya, H, Patterson, RD, Howard, MA 3rd, Friston, KJ, Griffiths, TD (2011). Predictive coding and pitch processing in the auditory cortex. Journal of Cognitive Neuroscience 23, 3084–3094.CrossRefGoogle ScholarPubMed
Laukka, P (2005). Categorical perception of vocal emotion expressions. Emotion 5, 277–295.CrossRefGoogle ScholarPubMed
Leitman, DI, Foxe, JJ, Butler, PD, Saperstein, A, Revheim, N, Javitt, DC (2005). Sensory contributions to impaired prosodic processing in schizophrenia. Biological Psychiatry 58, 56–61.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lenz, D, Schadow, J, Thaerig, S, Busch, NA, Herrmann, CS (2007). What's that sound? Matches with auditory long-term memory induce gamma activity in human EEG. International Journal of Psychophysiology 64, 31–38.CrossRefGoogle ScholarPubMed
Liu, T, Pinheiro, AP, Guanghui, D, Nestor, PG, McCarley, RW, Niznikiewicz, M (2012). Electrophysiological insights into processing nonverbal emotional vocalizations. Neuroreport 23, 108–112.CrossRefGoogle ScholarPubMed
Loughland, CM, Williams, LM, Gordon, E (2002). Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample. Schizophrenia Research 55, 159–170.CrossRefGoogle Scholar
Marmel, F, Perrin, F, Tillmann, B (2011). Tonal expectations influence early pitch processing. Journal of Cognitive Neuroscience 23, 3095–3104.CrossRefGoogle ScholarPubMed
Mitchell, RL, Elliott, R, Barry, M, Cruttenden, A, Woodruff, PW (2003). The neural response to emotional prosody, as revealed by functional magnetic resonance imaging. Neuropsychologia 41, 1410–1421.CrossRefGoogle ScholarPubMed
Niznikiewicz, M, Mittal, MS, Nestor, PG, McCarley, RW (2010). Abnormal inhibitory processes in semantic networks in schizophrenia. International Journal of Psychophysiology 75, 133–140.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Paulmann, S, Kotz, SA (2008 a). An ERP investigation on the temporal dynamics of emotional prosody and emotional semantics in pseudo- and lexical-sentence context. Brain and Language 105, 59–69.CrossRefGoogle ScholarPubMed
Paulmann, S, Kotz, SA (2008 b). Early emotional prosody perception based on different speaker voices. Neuroreport 19, 209–213.CrossRefGoogle ScholarPubMed
Paulmann, S, Seifert, S, Kotz, SA (2009). Orbito-frontal lesions cause impairment during late but not early emotional prosodic processing. Social Neuroscience 5, 59–75.CrossRefGoogle Scholar
Pinheiro, AP, Galdo-Alvarez, S, Rauber, A, Sampaio, A, Niznikiewicz, M, Goncalves, OF (2011). Abnormal processing of emotional prosody in Williams syndrome: an event-related potentials study. Research in Developmental Disabilities 32, 133–147.CrossRefGoogle ScholarPubMed
Poole, JH, Tobias, FC, Vinogradov, S (2000). The functional relevance of affect recognition errors in schizophrenia. Journal of the International Neuropsychological Society 6, 649–658.CrossRefGoogle ScholarPubMed
Ramus, F, Mehler, J (1999). Language identification with suprasegmental cues: a study based on speech resynthesis. Journal of the Acoustical Society of America 105, 512–521.CrossRefGoogle ScholarPubMed
Rauschecker, JP (1997). Processing of complex sounds in the auditory cortex of cat, monkey, and man. Acta Otolaryngological Supplementum 532, 34–38.CrossRefGoogle ScholarPubMed
Rosburg, T, Boutros, NN, Ford, JM (2008). Reduced auditory evoked potential component N100 in schizophrenia – a critical review. Psychiatry Research 161, 259–274.CrossRefGoogle ScholarPubMed
Ross, ED, Orbelo, DM, Cartwright, J, Hansel, S, Burgard, M, Testa, JA, Buck, R (2001). Affective-prosodic deficits in schizophrenia: comparison to patients with brain damage and relation to schizophrenic symptoms. Journal of Neurology, Neurosurgery and Psychiatry 70, 597–604.CrossRefGoogle ScholarPubMed
Rossell, SL, Batty, RA, Hughes, L (2010). Impaired semantic memory in the formation and maintenance of delusions post-traumatic brain injury: a new cognitive model. European Archives of Psychiatry and Clinical Neuroscience 260, 571–581.CrossRefGoogle ScholarPubMed
Rossell, SL, Boundy, CL (2005). Are auditory-verbal hallucinations associated with auditory affective processing deficits? Schizophrenia Research 78, 95–106.CrossRefGoogle ScholarPubMed
Sauter, SA, Eimer, M (2010). Rapid detection of emotion from human vocalizations. Journal of Cognitive Neuroscience 22, 474–481.CrossRefGoogle ScholarPubMed
Schadow, J, Lenz, D, Dettler, N, Frund, I, Hermann, CS (2009). Early gamma-band responses reflect anticipatory top-down modulation in the auditory cortex. Neuroimage 47, 651–658.CrossRefGoogle ScholarPubMed
Scherer, KR (1995). Expression of emotion in voice and music. Journal of Voice 9, 235–248.CrossRefGoogle ScholarPubMed
Schirmer, A, Kotz, SA (2006). Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing. Trends in Cognitive Sciences 10, 24–30.CrossRefGoogle ScholarPubMed
Scholten, MR, Aleman, A, Kahn, RS (2008). The processing of emotional prosody and semantics in schizophrenia: relationship to gender and IQ. Psychological Medicine 38, 887–898.CrossRefGoogle ScholarPubMed
Seiferth, NY, Pauly, K, Habel, U, Kellermann, T, Shah, NJ, Ruhrmann, S, Klosterkotter, J, Schneider, F, Kircher, T (2008). Increased neural response related to neutral faces in individuals at risk for psychosis. Neuroimage 40, 289–297.CrossRefGoogle ScholarPubMed
Seither-Preisler, A, Patterson, R, Krumbholz, K, Seither, S, Lutkenhoner, B (2006). Evidence of pitch processing in the N100m component of the auditory evoked field. Hearing Research 213, 88–98.CrossRefGoogle ScholarPubMed
Shaw, RJ, Dong, M, Lim, KO, Faustman, WO, Pouget, ER, Alpert, M (1999). The relationship between affect expression and affect recognition in schizophrenia. Schizophrenia Research 37, 245–250.CrossRefGoogle ScholarPubMed
Shea, TL, Sergejew, AA, Burnham, D, Jones, C, Rossell, SL, Copolov, DL, Egan, GF (2007). Emotional prosodic processing in auditory hallucinations. Schizophrenia Research 90, 214–220.CrossRefGoogle ScholarPubMed
Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW (2001). A review of MRI findings in schizophrenia. Schizophrenia Research 49, 1–52.CrossRefGoogle ScholarPubMed
Stufflebeam, SM, Poeppel, D, Rowley, HA, Roberts, TPL (1998). Peri-threshold encoding of stimulus frequency and intensity in the M100 latency. NeuroReport 9, 91–94.CrossRefGoogle ScholarPubMed
Turetsky, BI, Bilker, WB, Siegel, SJ, Kohler, CG, Gur, RE (2009). Profile of auditory information-processing deficits in schizophrenia. Psychiatry Research 165, 27–37.CrossRefGoogle ScholarPubMed
Wechsler, D (1997). Wechsler Adult Intelligence Scale: Administration and Scoring Manual, 3rd edn.. The Psychological Corporation: San Antonio, TX.Google Scholar
Wible, CG, Preus, AP, Hashimoto, R (2009). A cognitive neuroscience view of schizophrenic symptoms: abnormal activation of a system for social perception and communication. Brain Imaging and Behavior 3, 85–110.CrossRefGoogle ScholarPubMed
Wildgruber, D, Ackermann, H, Kreifelts, B, Ethofer, T (2006). Cerebral processing of linguistic and emotional prosody: fMRI studies. Progress in Brain Research 156, 249–268.CrossRefGoogle ScholarPubMed
Wildgruber, D, Riecker, A, Hertrich, I, Erb, M, Grodd, W, Ethofer, T, Ackermann, H (2005). Identification of emotional intonation evaluated by fMRI. Neuroimage 24, 1233–1241.CrossRefGoogle ScholarPubMed