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

  • A. P. Pinheiro (a1) (a2), E. del Re (a2), J. Mezin (a2), P. G. Nestor (a2) (a3), A. Rauber (a4), R. W. McCarley (a2), Ó. F. Gonçalves (a1) and M. A. Niznikiewicz (a2)...



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.


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.


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.


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.


Corresponding author

*Address for correspondence: M. Niznikiewicz, Ph.D., Department of Psychiatry-116A, Boston VA Healthcare System, 940 Belmont Street, Brockton, MA 02301, USA. (Email:


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American Electroencephalographic Society (1991). Guidelines for standard electrode position nomenclature. Journal of Clinical Neurophysiology 8, 200202.
APA (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn, revised. APA: Washington, DC.
Baltaxe, CA, Simmons, JQ III (1995). Speech and language disorders in children and adolescents with schizophrenia. Schizophrenia Bulletin 21, 677692.
Banse, R, Scherer, KR (1996). Acoustic profiles in vocal emotion expression. Journal of Personality and Social Psychology 70, 614636.
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, 8185.
Brekke, J, Kay, DD, Lee, KS, Green, MF (2005). Biosocial pathways to functional outcome in schizophrenia. Schizophrenia Research 80, 213225.
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, 227238.
Chandrasekaran, B, Krishnan, A, Gandour, JT (2009). Sensory processing of linguistic pitch as reflected by the mismatch negativity. Ear and Hearing 30, 552558.
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, 5868.
Crowley, KE, Colrain, IM (2004). A review of the evidence for P2 being an independent component process: age, sleep and modality. Clinical Neurophysiology 115, 732744.
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, 118123.
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, 13931396.
Edwards, J, Pattison, PE, Jackson, HJ, Wales, RJ (2001). Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophrenia Research 48, 235253.
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, 580587.
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.
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.
Forces, RB, Venables, NC, Sponheim, SR (2008). An auditory processing abnormality specific to liability for schizophrenia. Schizophrenia Research 103, 298310.
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, 149157.
Garety, PA, Kuipers, E, Fowler, D, Freeman, D, Bebbington, PE (2001). A cognitive model of the positive symptoms of psychosis. Psychological Medicine 31, 189195.
Gonsalvez, CJ, Barry, RJ, Rushby, JA, Polich, J (2007). Target-to-target interval, intensity, and P300 from an auditory single-stimulus task. Psychophysiology 44, 245250.
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, 145146.
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, 119136.
Green, MJ, Williams, LM, Davidson, D (2003). Visual scanpaths to threat-related faces in deluded schizophrenia. Psychiatry Research 3, 271285.
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, 104112.
Haskins, B, Shutty, MS, Kellogg, E (1995). Affect processing in chronically psychotic patients: development of a reliable assessment tool. Schizophrenia Research 15, 291297.
Hillyard, SA, Hink, RF, Schwent, VL, Picton, TW (1973). Electrical signs of selective attention in the human brain. Science 182, 177180.
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, 135145.
Hollingshead, AB (1965). Two-Factor Index of Social Position. Yale Station: New Haven, CT.
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, 247256.
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, 8391.
Kay, SR, Fiszbein, A, Opler, LA (1987). The Positive and Negative Syndrome Scale (PANSS). Schizophrenia Bulletin 13, 261276.
Kerr, SL, Neale, JM (1993). Emotion perception in schizophrenia: specific deficit or further evidence of generalized poor performance? Journal of Abnormal Psychology 102, 312318.
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, 366376.
Kotz, SA, Paulmann, S (2007). When emotional prosody and semantics dance cheek to cheek: ERP evidence. Brain Research 1151, 107118.
Krishnan, RR, Keefe, R, Kraus, M (2009). Schizophrenia is a disorder of higher order hierarchical processing. Medical Hypotheses 6, 740744.
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, 523528.
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, 30843094.
Laukka, P (2005). Categorical perception of vocal emotion expressions. Emotion 5, 277295.
Leitman, DI, Foxe, JJ, Butler, PD, Saperstein, A, Revheim, N, Javitt, DC (2005). Sensory contributions to impaired prosodic processing in schizophrenia. Biological Psychiatry 58, 5661.
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, 545556.
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, 611618.
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, 3138.
Liu, T, Pinheiro, AP, Guanghui, D, Nestor, PG, McCarley, RW, Niznikiewicz, M (2012). Electrophysiological insights into processing nonverbal emotional vocalizations. Neuroreport 23, 108112.
Loughland, CM, Williams, LM, Gordon, E (2002). Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample. Schizophrenia Research 55, 159170.
Marmel, F, Perrin, F, Tillmann, B (2011). Tonal expectations influence early pitch processing. Journal of Cognitive Neuroscience 23, 30953104.
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, 14101421.
Niznikiewicz, M, Mittal, MS, Nestor, PG, McCarley, RW (2010). Abnormal inhibitory processes in semantic networks in schizophrenia. International Journal of Psychophysiology 75, 133140.
Oldfield, RC (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia 9, 97113.
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, 5969.
Paulmann, S, Kotz, SA (2008 b). Early emotional prosody perception based on different speaker voices. Neuroreport 19, 209213.
Paulmann, S, Seifert, S, Kotz, SA (2009). Orbito-frontal lesions cause impairment during late but not early emotional prosodic processing. Social Neuroscience 5, 5975.
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, 133147.
Poole, JH, Tobias, FC, Vinogradov, S (2000). The functional relevance of affect recognition errors in schizophrenia. Journal of the International Neuropsychological Society 6, 649658.
Ramus, F, Mehler, J (1999). Language identification with suprasegmental cues: a study based on speech resynthesis. Journal of the Acoustical Society of America 105, 512521.
Rauschecker, JP (1997). Processing of complex sounds in the auditory cortex of cat, monkey, and man. Acta Otolaryngological Supplementum 532, 3438.
Rosburg, T, Boutros, NN, Ford, JM (2008). Reduced auditory evoked potential component N100 in schizophrenia – a critical review. Psychiatry Research 161, 259274.
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, 597604.
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, 571581.
Rossell, SL, Boundy, CL (2005). Are auditory-verbal hallucinations associated with auditory affective processing deficits? Schizophrenia Research 78, 95106.
Sauter, SA, Eimer, M (2010). Rapid detection of emotion from human vocalizations. Journal of Cognitive Neuroscience 22, 474481.
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, 651658.
Scherer, KR (1995). Expression of emotion in voice and music. Journal of Voice 9, 235248.
Schirmer, A, Kotz, SA (2006). Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing. Trends in Cognitive Sciences 10, 2430.
Scholten, MR, Aleman, A, Kahn, RS (2008). The processing of emotional prosody and semantics in schizophrenia: relationship to gender and IQ. Psychological Medicine 38, 887898.
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, 289297.
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, 8898.
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, 245250.
Shea, TL, Sergejew, AA, Burnham, D, Jones, C, Rossell, SL, Copolov, DL, Egan, GF (2007). Emotional prosodic processing in auditory hallucinations. Schizophrenia Research 90, 214220.
Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW (2001). A review of MRI findings in schizophrenia. Schizophrenia Research 49, 152.
Stufflebeam, SM, Poeppel, D, Rowley, HA, Roberts, TPL (1998). Peri-threshold encoding of stimulus frequency and intensity in the M100 latency. NeuroReport 9, 9194.
Turetsky, BI, Bilker, WB, Siegel, SJ, Kohler, CG, Gur, RE (2009). Profile of auditory information-processing deficits in schizophrenia. Psychiatry Research 165, 2737.
Wechsler, D (1997). Wechsler Adult Intelligence Scale: Administration and Scoring Manual, 3rd edn.. The Psychological Corporation: San Antonio, TX.
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, 85110.
Wildgruber, D, Ackermann, H, Kreifelts, B, Ethofer, T (2006). Cerebral processing of linguistic and emotional prosody: fMRI studies. Progress in Brain Research 156, 249268.
Wildgruber, D, Riecker, A, Hertrich, I, Erb, M, Grodd, W, Ethofer, T, Ackermann, H (2005). Identification of emotional intonation evaluated by fMRI. Neuroimage 24, 12331241.


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

  • A. P. Pinheiro (a1) (a2), E. del Re (a2), J. Mezin (a2), P. G. Nestor (a2) (a3), A. Rauber (a4), R. W. McCarley (a2), Ó. F. Gonçalves (a1) and M. A. Niznikiewicz (a2)...


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