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Deficient auditory predictive coding during vocalization in the psychosis risk syndrome and in early illness schizophrenia: the final expanded sample

Published online by Cambridge University Press:  25 September 2018

Daniel H Mathalon ,
Brian J Roach ,
Jamie M Ferri ,
Rachel L Loewy ,
Barbara K Stuart ,
Veronica B Perez ,
Tara H Trujillo  and
Judith M Ford Open the ORCID record for Judith M Ford [Opens in a new window]
Daniel H Mathalon
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA 94121, USA
Brian J Roach
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA 94121, USA
Jamie M Ferri
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA
Rachel L Loewy
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA
Barbara K Stuart
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA
Veronica B Perez
Affiliation:
California School of Professional Psychology (CSPP), Alliant International University, San Diego, CA, USA University of California, San Diego (UCSD), La Jolla, CA, USA
Tara H Trujillo
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA 94121, USA
Judith M Ford*
Affiliation:
University of California, San Francisco (UCSF), San Francisco, CA, USA Veterans Affairs San Francisco Healthcare System, San Francisco, CA 94121, USA
*
Author for correspondence: Judith M. Ford, E-mail: Judith.ford@ucsf.edu
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Abstract

Background

During vocalization, efference copy/corollary discharge mechanisms suppress the auditory cortical response to self-generated sounds. Previously, we found attenuated vocalization-related auditory cortical suppression in psychosis and a similar trend in the psychosis risk syndrome. Here, we report data from the final sample of early illness schizophrenia patients (ESZ), individuals at clinical high risk for psychosis (CHR), and healthy controls (HC).

Methods

Event-related potentials (ERP) were recorded from ESZ (n = 84), CHR (n = 71), and HC (n = 103) participants during a vocalization paradigm. The N1 ERP component was elicited during production (Talk) and playback (Listen) of vocalization. Age effects on N1 suppression (Talk–Listen), Talk N1, and Listen N1 were compared across groups. N1 measures were adjusted for normal aging before testing for group differences.

Results

Both ESZ and CHR groups showed reduced Talk–Listen N1 suppression relative to HC, but did not differ from each other. Listen N1 was reduced in ESZ, but not in CHR, relative to HC. Deficient Talk–Listen N1 suppression was associated with greater unusual thought content in CHR individuals. N1 suppression increased with age in HC (12–36 years), and while CHR individuals showed a similar age-related increase, no such relationship was evident in ESZ.

Conclusions

Putative efference copy/corollary discharge-mediated auditory cortical suppression during vocalization is deficient in ESZ and precedes psychosis onset, particularly in CHR individuals with greater unusual thought content. Furthermore, this suppression increases from adolescence through early adulthood, likely reflecting the effects of normal brain maturation. This maturation effect is disrupted in ESZ, presumably due to countervailing illness effects.

Keywords

Clinical high-riskcorollary dischargeN1psychosisvocalization
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 11 , August 2019 , pp. 1897 - 1904
Creative Commons
Parts of this are a work of the U.S. Government and not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2018

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References

Addington, J, Liu, L, Buchy, L, Cadenhead, KS, Cannon, TD, Cornblatt, BA, Perkins, DO, Seidman, LJ, Tsuang, MT, Walker, EF, Woods, SW, Bearden, CE, Mathalon, DH and Mcglashan, TH (2015) North American prodrome Longitudinal Study (NAPLS 2): the prodromal symptoms. Journal of Nervous and Mental Diseases 203, 328–335.Google Scholar
Andreasen, NC (1984) Scale for the Assessment of Positive Symptoms. Iowa City, IA: University of Iowa.Google Scholar
Blakemore, SJ, Smith, J, Steel, R, Johnstone, CE and Frith, CD (2000) The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: evidence for a breakdown in self-monitoring. Psychological Medicine 30, 1131–1139.Google Scholar
Brebion, G, Amador, X, David, AS, Malaspina, D, Sharif, Z and Gorman, JM (2000) Positive symptomatology and source-monitoring failure in schizophrenia – an analysis of symptom-specific effects. Psychiatry Research 95, 119–131.Google Scholar
Burnett, TA, Freedland, MB, Larson, CR and Hain, TC (1998) Voice F0 responses to manipulations in pitch feedback. Journal of the Acoustical Society of America 103, 3153–3161.Google Scholar
Cannon, TD, Cadenhead, K, Cornblatt, B, Woods, SW, Addington, J, Walker, E, Seidman, LJ, Perkins, D, Tsuang, M, Mcglashan, T and Heinssen, R (2008) Prediction of psychosis in youth at high clinical risk: a multisite longitudinal study in North America. Archives of General Psychiatry 65, 28–37.Google Scholar
Chen, CM, Mathalon, DH, Roach, BJ, Cavus, I, Spencer, DD and Ford, JM (2011) The corollary discharge in humans is related to synchronous neural oscillations. Journal of Cognitive Neuroscience 23, 2892–2904.Google Scholar
Crapse, TB and Sommer, MA (2008) Corollary discharge across the animal kingdom. Nature Reviews Neuroscience 9, 587–600.Google Scholar
Curio, G, Neuloh, G, Numminen, J, Jousmaki, V and Hari, R (2000) Speaking modifies voice-evoked activity in the human auditory cortex. Human Brain Mapping 9, 183–191.Google Scholar
De Clercq, W, Vergult, A, Vanrumste, B, Van Paesschen, W and Van Huffel, S (2006) Canonical correlation analysis applied to remove muscle artifacts from the electroencephalogram. Institute of Electrical and Electronics Engineers Transactions in Biomedical Engineering 53, 2583–2587.Google Scholar
Delorme, A and Makeig, S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods 134, 9–21.Google Scholar
Eliades, SJ and Wang, X (2003) Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. Journal of Neurophysiology 89, 2194–2207.Google Scholar
Eliades, SJ and Wang, X (2005) Dynamics of auditory-vocal interaction in monkey auditory cortex. Cerebral Cortex 15, 1510–1523.Google Scholar
Feinberg, I (1978) Efference copy and corollary discharge: implications for thinking and its disorders. Schizophrenia Bulletin 4, 636–640.Google Scholar
Feinberg, I and Guazzelli, M (1999) Schizophrenia – a disorder of the corollary discharge systems that integrate the motor systems of thought with the sensory systems of consciousness. British Journal of Psychiatry 174, 196–204.Google Scholar
First, MB, Spitzer, RL, Gibbon, M and Williams, JB (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCIP-I/P), New York State Psychiatric Institute, New York.Google Scholar
Ford, JM and Mathalon, DH (2005) Corollary discharge dysfunction in schizophrenia: can it explain auditory hallucinations? International Journal of Psychophysiology 58, 179–189.Google Scholar
Ford, JM and Mathalon, DH (2012) Anticipating the future: automatic prediction failures in schizophrenia. International Journal of Psychophysiology 83, 232–239.Google Scholar
Ford, JM, Mathalon, DH, Heinks, T, Kalba, S and Roth, WT (2001) Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. American Journal of Psychiatry 158, 2069–2071.Google Scholar
Ford, JM, Gray, M, Faustman, WO, Roach, BJ and Mathalon, DH (2007 a) Dissecting corollary discharge dysfunction in schizophrenia. Psychophysiology 44, 522–529.Google Scholar
Ford, JM, Roach, BJ, Faustman, WO and Mathalon, DH (2007 b) Synch before you speak: auditory hallucinations in schizophrenia. American Journal of Psychiatry 164, 458–466.Google Scholar
Ford, JM, Roach, BJ and Mathalon, DH (2010) Assessing corollary discharge in humans using noninvasive neurophysiological methods. Nature Protocols 5, 1160–1168.Google Scholar
Ford, JM, Mathalon, DH, Roach, BJ, Keedy, SK, Reilly, JL, Gershon, ES and Sweeney, JA (2013) Neurophysiological evidence of corollary discharge function during vocalization in psychotic patients and their nonpsychotic first-degree relatives. Schizophrenia Bulletin 39, 1272–1280.Google Scholar
Frith, CD, Blakemore, SJ and Wolpert, DM (2000) Abnormalities in the awareness and control of action. Philosophical Transactions of the Royal Society B: Biological Sciences 355, 1771–1788.Google Scholar
Greenlee, JD, Jackson, AW, Chen, F, Larson, CR, Oya, H, Kawasaki, H, Chen, H and Howard, MA 3rd (2011) Human auditory cortical activation during self-vocalization. Public Library of Science One 6, e14744.Google Scholar
Heinks-Maldonado, TH, Mathalon, DH, Gray, M and Ford, JM (2005) Fine-tuning of auditory cortex during speech production. Psychophysiology 42, 180–190.Google Scholar
Heinks-Maldonado, TH, Nagarajan, SS and Houde, JF (2006) Magnetoencephalographic evidence for a precise forward model in speech production. Neuroreport 17, 1375–1379.Google Scholar
Heinks-Maldonado, TH, Mathalon, DH, Houde, JF, Gray, M, Faustman, WO and Ford, JM (2007) Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations. Archives of General Psychiatry 64, 286–296.Google Scholar
Houde, JF and Jordan, MI (1998) Sensorimotor adaptation in speech production. Science 279, 1213–1216.Google Scholar
Houde, JF and Jordan, MI (2002) Sensorimotor adaptation of speech I: compensation and adaptation. Journal of Speech, Language, and Hearing Research 45, 295–310.Google Scholar
Houde, JF and Nagarajan, SS (2011) Speech production as state feedback control. Frontiers of Human Neuroscience 5, 82.Google Scholar
Houde, JF, Nagarajan, SS, Sekihara, K and Merzenich, MM (2002) Modulation of the auditory cortex during speech: an MEG study. Journal of Cognitive Neuroscience 14, 1125–1138.Google Scholar
Howell, DC (2017) Fundamental Statistics for the Behavioral Sciences. Cengage Learning, Boston, MA, USA, 9th edition.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, and Ryan, N (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980–988.Google Scholar
Kayser, J and Tenke, CE (2003) Optimizing PCA methodology for ERP component identification and measurement: theoretical rationale and empirical evaluation. Clinical Neurophysiology 114, 2307–2325.Google Scholar
Leonowicz, Z, Karvanen, J and Shishkin, SL (2005) Trimmed estimators for robust averaging of event-related potentials. Journal of Neuroscience Methods 142, 17–26.Google Scholar
Lindner, A, Thier, P, Kircher, TT, Haarmeier, T and Leube, DT (2005) Disorders of agency in schizophrenia correlate with an inability to compensate for the sensory consequences of actions. Current Biology 15, 1119–1124.Google Scholar
Mathalon, DH and Ford, JM (2008) Corollary discharge dysfunction in schizophrenia: evidence for an elemental deficit. Clinical EEG and Neuroscience 39, 82–86.Google Scholar
Miller, TJ, Mcglashan, TH, Rosen, JL, Somjee, L, Markovich, PJ, Stein, K and Woods, SW (2002) Prospective diagnosis of the initial prodrome for schizophrenia based on the Structured Interview for Prodromal Syndromes: preliminary evidence of interrater reliability and predictive validity. American Journal of Psychiatry 159, 863–865.Google Scholar
Miller, TJ, Mcglashan, TH, Rosen, JL, Cadenhead, K, Cannon, T, Ventura, J, Mcfarlane, W, Perkins, DO, Pearlson, GD and Woods, SW (2003) Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophrenia Bulletin 29, 703–715.Google Scholar
Nolan, H, Whelan, R and Reilly, RB (2010) FASTER: fully automated statistical thresholding for EEG artifact rejection. Journal of Neuroscience Methods 192, 152–162.Google Scholar
Pardo, JS (2006) On phonetic convergence during conversational interaction. The Journal of the Acoustical Society of America 119, 2382.Google Scholar
Perez, VB, Ford, JM, Roach, BJ, Loewy, RL, Stuart, BK, Vinogradov, S and Mathalon, DH (2012) Auditory cortex responsiveness during talking and listening: early illness schizophrenia and patients at clinical high-risk for psychosis. Schizophrenia Bulletin 38, 1216–1224.Google Scholar
Pfefferbaum, A, Wenegrat, BG, Ford, JM, Roth, WT and Kopell, BS (1984) Clinical application of the P3 component of event-related potentials. II. Dementia, depression and schizophrenia. Electroencephalography and Clinical Neurophysiology 59, 104–124.Google Scholar
Phillips, LJ, Yung, AR and Mcgorry, PD (2000) Identification of young people at risk of psychosis: validation of Personal Assessment and Crisis Evaluation Clinic intake criteria. Australian and New Zealand Journal Psychiatry 34(Suppl.), S164–S169.Google Scholar
Poulet, JF and Hedwig, B (2002) A corollary discharge maintains auditory sensitivity during sound production. Nature 418, 872–876.Google Scholar
Ries, S, Janssen, N, Burle, B and Alario, FX (2013) Response-locked brain dynamics of word production. Public Library of Science One 8, e58197.Google Scholar
Rosburg, T, Boutros, NN and Ford, JM (2008) Reduced auditory evoked potential component N100 in schizophrenia – a critical review. Psychiatry Research 161, 259–274.Google Scholar
Seal, ML, Aleman, A and Mcguire, PK (2004) Compelling imagery, unanticipated speech and deceptive memory: neurocognitive models of auditory verbal hallucinations in schizophrenia. Cognitive Neuropsychiatry 9, 43–72.Google Scholar
Sinai, A and Pratt, H (2002) Electrophysiological evidence for priming in response to words and pseudowords in first and second language. Brain and Language 80, 240–252.Google Scholar
Sitek, KR, Mathalon, DH, Roach, BJ, Houde, JF, Niziolek, CA and Ford, JM (2013) Auditory cortex processes variation in our own speech. Public Library of Science One, 8, e82925.Google Scholar
Von Holst, E and Mittelstaedt, H (1950) Das reafferenzprinzip. Naturwissenschaften 37, 464–476.Google Scholar
Wang, J, Mathalon, DH, Roach, BJ, Reilly, J, Keedy, SK, Sweeney, JA and Ford, JM (2014) Action planning and predictive coding when speaking. Neuroimage 91, 91–98.Google Scholar
Woods, SW, Addington, J, Cadenhead, KS, Cannon, TD, Cornblatt, BA, Heinssen, R, Perkins, DO, Seidman, LJ, Tsuang, MT, Walker, EF and Mcglashan, TH (2009) Validity of the prodromal risk syndrome for first psychosis: findings from the North American Prodrome Longitudinal Study. Schizophrenia Bulletin 35, 894–908.Google Scholar
Yung, A (2008) Prognostic factors for progression to psychosis in high risk youth. Evidence Based Mental Health 11, 72.Google Scholar
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