Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-18T04:34:48.477Z Has data issue: false hasContentIssue false
  • English
  • Français

Parsing components of auditory predictive coding in schizophrenia using a roving standard mismatch negativity paradigm

Published online by Cambridge University Press:  15 January 2019

Amanda McCleery ,
Daniel H. Mathalon ,
Jonathan K. Wynn ,
Brian J. Roach ,
Gerhard S. Hellemann ,
Stephen R. Marder  and
Michael F. Green
Amanda McCleery*
Affiliation:
Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, CA, USA
Daniel H. Mathalon
Affiliation:
Veterans Affairs San Francisco Healthcare System, San Francisco, CA, USA Department of Psychiatry, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
Jonathan K. Wynn
Affiliation:
Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, CA, USA
Brian J. Roach
Affiliation:
Veterans Affairs San Francisco Healthcare System, San Francisco, CA, USA
Gerhard S. Hellemann
Affiliation:
Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, CA, USA
Stephen R. Marder
Affiliation:
Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, CA, USA
Michael F. Green
Affiliation:
Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA, USA Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, CA, USA
*
Author for correspondence: Amanda McCleery, E-mail: amccleery@mednet.ucla.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Mismatch negativity (MMN) is an event-related potential (ERP) component reflecting auditory predictive coding. Repeated standard tones evoke increasing positivity (‘repetition positivity’; RP), reflecting strengthening of the standard's memory trace and the prediction it will recur. Likewise, deviant tones preceded by more standard repetitions evoke greater negativity (‘deviant negativity’; DN), reflecting stronger prediction error signaling. These memory trace effects are also evident in MMN difference wave. Here, we assess group differences and test-retest reliability of these indices in schizophrenia patients (SZ) and healthy controls (HC).

Methods

Electroencephalography was recorded twice, 2 weeks apart, from 43 SZ and 30 HC, during a roving standard paradigm. We examined ERPs to the third, eighth, and 33rd standards (RP), immediately subsequent deviants (DN), and the corresponding MMN. Memory trace effects were assessed by comparing amplitudes associated with the three standard repetition trains.

Results

Compared with controls, SZ showed reduced MMNs and DNs, but normal RPs. Both groups showed memory trace effects for RP, MMN, and DN, with a trend for attenuated DNs in SZ. Intraclass correlations obtained via this paradigm indicated good-to-moderate reliabilities for overall MMN, DN and RP, but moderate to poor reliabilities for components associated with short, intermediate, and long standard trains, and poor reliability of their memory trace effects.

Conclusion

MMN deficits in SZ reflected attenuated prediction error signaling (DN), with relatively intact predictive code formation (RP) and memory trace effects. This roving standard MMN paradigm requires additional development/validation to obtain suitable levels of reliability for use in clinical trials.

Keywords

deviant negativitymemory tracemismatch negativityprediction error signalingpredictive codingpsychotic disordersrepetition negativity
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 7 , May 2019 , pp. 1195 - 1206
Copyright
Copyright © Cambridge University Press 2019 

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

*

Co-first authors.

References

Adams, RA, Stephan, KE, Brown, HR, Frith, CD and Friston, KJ (2013) The computational anatomy of psychosis. Frontiers in Psychiatry 4, 1–26.Google Scholar
Alho, K (1995) Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes. Ear and Hearing 16, 38–51.Google Scholar
American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders, 4th Edn. (DSM-IV), Washington, DC: American Psychiatric Association.Google Scholar
Avissar, M, Xie, S, Vail, B, Lopez-Calderon, J, Wang, Y and Javitt, DC (2017) Meta-analysis of mismatch negativity to simple versus complex deviants in schizophrenia. Schizophrenia Research 191, 25–34.Google Scholar
Baldeweg, T (2007) ERP repetition effects and mismatch negativity generation: a predictive coding perspective. Journal of Psychophysiology 21, 204–213.Google Scholar
Baldeweg, T and Hirsch, SR (2015) Mismatch negativity indexes illness-specific impairments of cortical plasticity in schizophrenia: a comparison with bipolar disorder and Alzheimer's disease. International Journal of Psychophysiology 95, 145–155.Google Scholar
Baldeweg, T, Klugman, A, Gruzelier, J and Hirsch, SR (2004) Mismatch negativity potentials and cognitive impairment in schizophrenia. Schizophrenia Research 69, 203–217.Google Scholar
Baldeweg, T, Wong, D and Stephan, KE (2006) Nicotinic modulation of human auditory sensory memory: evidence from mismatch negativity potentials. International Journal of Psychophysiology 59, 49–58.Google Scholar
Benjamin, L (1994) Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID II). New York, NY: Biometric Research Department, New York: State Psychiatric Institute.Google Scholar
Biagianti, B, Roach, BJ, Fisher, M, Loewy, R, Ford, JM, Vinogradov, S and Mathalon, DH (2017) Trait aspects of auditory mismatch negativity predict response to auditory training in individuals with early illness schizophrenia. Neuropsychiatric Electrophysiology 3, 2.Google Scholar
Bodatsch, M, Ruhrmann, S, Wagner, M, Müller, R, Schultze-Lutter, F, Frommann, I, Brinkmeyer, J, Gaebel, W, Maier, W, Klosterkötter, J and Brockhaus-Dumke, A (2011) Prediction of psychosis by mismatch negativity. Biological Psychiatry 69, 959–966.Google Scholar
Breen, EC, Perez, C, Olmstead, R, Eisenberger, N and Irwin, MR (2014) 135. Comparison of multiplex immunoassays and ELISAs for the determination of circulating levels of inflammatory cytokines. Brain, Behavior, and Immunity 40, e39.Google Scholar
Cowan, N, Winkler, I, Teder, W and Naatanen, R (1993) Memory prerequisites of mismatch negativity in the auditory event-related potential (ERP). Journal of Experimental Psychology: Learning, Memory, and Cognition 19, 909–921.Google Scholar
Csépe, V (1995) On the origin and development of the mismatch negativity. Ear and Hearing 16, 91–104.Google Scholar
Deouell, LY, Bentin, S and Giard, M-H (1998) Mismatch negativity in dichotic listening: evidence for interhemispheric differences and multiple generators. Psychophysiology 35, 355–365.Google Scholar
Erickson, MA, Ruffle, A and Gold, JM (2016) A meta-analysis of mismatch negativity in schizophrenia: from clinical risk to disease specificity and progression. Biological Psychiatry 79, 980–987.Google Scholar
First, M and Gibbon, M (2004) The structured clinical interview for DSM-IV axis I disorders (SCID-I) and the structured clinical interview for DSM-IV axis II disorders (SCID-II). In Hilsenroth, MJ and Segal, DL (eds), Comprehensive Handbook of Psychological Assessment, vol. 2. Personality assessment. Hoboken, NJ, USA: John Wiley & Sons Inc, pp. 134–143.Google Scholar
First, M, Williams, J, Karg, R and Spitzer, R (2014) Structured Clinical Interview for DSM-5 Disorders (SCID-5), Research Version. Arlington, VA: American Psychiatric Association.Google Scholar
Fletcher, PC and Frith, CD (2009) Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nature Reviews Neuroscience 10, 48–58.Google Scholar
Friedman, T, Sehatpour, P, Dias, E, Perrin, M and Javitt, DC (2012) Differential relationships of mismatch negativity and visual P1 deficits to premorbid characteristics and functional outcome in schizophrenia. Biological Psychiatry 71, 521–529.Google Scholar
Friston, K (2005) A theory of cortical responses. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 815–836.Google Scholar
Friston, KJ, Stephan, KE, Montague, R and Dolan, RJ (2014) Computational psychiatry: the brain as a phantastic organ. The Lancet Psychiatry 1, 148–158.Google Scholar
Garrido, MI, Kilner, JM, Kiebel, SJ, Stephan, KE, Baldeweg, T and Friston, KJ (2009 a) Repetition suppression and plasticity in the human brain. Neuroimage 48, 269–279.Google Scholar
Garrido, MI, Kilner, JM, Stephan, KE and Friston, KJ (2009 b) The mismatch negativity: a review of underlying mechanisms. Clinical Neurophysiology 120, 453–463.Google Scholar
Giard, M, Perrin, F, Pernier, J and Bouchet, P (1990) Brain generators implicated in the processing of auditory stimulus deviance: a topographic event-related potential study. Psychophysiology 27, 627–640.Google Scholar
Goodman, SH, Sewell, DR, Cooley, EL and Leavitt, N (1993) Assessing levels of adaptive functioning: the role functioning scale. Community Mental Health Journal 29, 119–131.Google Scholar
Haenschel, C, Vernon, DJ, Dwivedi, P, Gruzelier, JH and Baldeweg, T (2005) Event-related brain potential correlates of human auditory sensory memory-trace formation. Journal of Neuroscience 25, 10494–10501.Google Scholar
Haigh, SM, Coffman, BA and Salisbury, DF (2017) Mismatch negativity in first-episode schizophrenia. Clinical EEG and Neuroscience 48, 3–10.Google Scholar
Hall, MH, Schulze, K, Rijsdijk, F, Picchioni, M, Ettinger, U, Bramon, E, Freedman, R, Murray, RM and Sham, P (2006) Heritability and reliability of P300, P50 and duration mismatch negativity. Behavior Genetics 36, 845–857.Google Scholar
Hamilton, HK, Perez, VB, Ford, JM, Roach, BJ, Jaeger, J and Mathalon, DH (2017) Mismatch negativity but not P300 Is associated with functional disability in schizophrenia. Schizophrenia Bulletin 44, 492–504.Google Scholar
Hay, RA, Roach, BJ, Srihari, VH, Woods, SW, Ford, JM and Mathalon, DH (2015) Equivalent mismatch negativity deficits across deviant types in early illness schizophrenia-spectrum patients. Biological Psychology 105C, 130–137.Google Scholar
Heilbron, M and Chait, M (2017) Great expectations: is there evidence for predictive coding in auditory cortex? Neuroscience 389, 54–73.Google Scholar
Horga, G, Schatz, KC, Abi-Dargham, A and Peterson, BS (2014) Deficits in predictive coding underlie hallucinations in schizophrenia. Journal of Neuroscience 34, 8072–8082.Google Scholar
Javitt, DC, Grochowski, S, Shelley, AM and Ritter, W (1998) Impaired mismatch negativity (MMN) generation in schizophrenia as a function of stimulus deviance, probability, and interstimulus/interdeviant interval. Electroencephalography and Clinical Neurophysiology 108, 143–153.Google Scholar
Kiang, M, Light, GA, Prugh, J, Coulson, S, Braff, DL and Kutas, M (2007) Cognitive, neurophysiological, and functional correlates of proverb interpretation abnormalities in schizophrenia. Journal of the International Neuropsychological Society 13, 653–663.Google Scholar
Kring, AM, Gur, RE, Blanchard, JJ, Horan, WP and Reise, SP (2013) The Clinical Assessment Interview for Negative Symptoms (CAINS): final development and validation. American Journal of Psychiatry 170, 165–172.Google Scholar
Lalanne, L, Van Assche, M and Giersch, A (2012) When predictive mechanisms go wrong: disordered visual synchrony thresholds in schizophrenia. Schizophrenia Bulletin 38, 506–513.Google Scholar
Levanen, S, Hari, R, McEvoy, L and Sams, M (1993) Responses of the human auditory cortex to changes in one versus two stimulus features. Experimental Brain Research 97, 177–183.Google Scholar
Lew, HL, Gray, M and Poole, JH (2007) Temporal stability of auditory event-related potentials in healthy individuals and patients with traumatic brain injury. Journal of Clinical Neurophysiology 24, 392–397.Google Scholar
Light, GA and Braff, DL (2005) Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Archives of General Psychiatry 62, 127–136.Google Scholar
Light, GA, Swerdlow, NR, Rissling, AJ, Radant, A, Sugar, CA, Sprock, J, Pela, M, Geyer, MA and Braff, DL (2012) Characterization of neurophysiologic and neurocognitive biomarkers for use in genomic and clinical outcome studies of schizophrenia. PLoS ONE 7, e39434.Google Scholar
Light, GA, Swerdlow, NR, Thomas, ML, Calkins, ME, Green, MF, Greenwood, TA, Gur, RE, Gur, RC, Lazzeroni, LC, Nuechterlein, KH, Pela, M, Radant, AD, Seidman, LJ, Sharp, RF, Siever, LJ, Silverman, JM, Sprock, J, Stone, WS, Sugar, CA, Tsuang, DW, Tsuang, MT, Braff, DL and Turetsky, BI (2015) Validation of mismatch negativity and P3a for use in multi-site studies of schizophrenia: characterization of demographic, clinical, cognitive, and functional correlates in COGS-2. Schizophrenia Research 163, 63–72.Google Scholar
Lukoff, D, Nuechterlein, KH and Ventura, J (1986) Manual for the expanded brief psychiatric rating scale. Schizophrenia Bulletin 12, 594–602.Google Scholar
Michie, PT, Budd, TW, Todd, J, Rock, D, Wichmann, H, Box, J and Jablensky, AV (2000) Duration and frequency mismatch negativity in schizophrenia. Clinical Neurophysiology 111, 1054–1065.Google Scholar
Molholm, S, Martinez, A, Ritter, W, Javitt, DC and Foxe, JJ (2004) The neural circuitry of pre-attentive auditory change-detection: an fMRI study of pitch and duration mismatch negativity generators. Cerebral Cortex 15, 545–551.Google Scholar
Näätänen, R (2008) Mismatch negativity (MMN) as an index of central auditory system plasticity. International Journal of Audiology 47, S16–S20.Google Scholar
Näätänen, R and Kähkönen, S (2009) Central auditory dysfunction in schizophrenia as revealed by the mismatch negativity (MMN) and its magnetic equivalent MMNm: a review. International Journal of Neuropsychopharmacology 12, 125–135.Google Scholar
Näätänen, R, Paavilainen, P, Rinne, T and Alho, K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clinical Neurophysiology 118, 2544–2590.Google Scholar
Nagai, T, Tada, M, Kirihara, K, Yahata, N, Hashimoto, R, Araki, T and Kasai, K (2013) Auditory mismatch negativity and P3a in response to duration and frequency changes in the early stages of psychosis. Schizophrenia Research 150, 547–554.Google Scholar
Nazimek, JM, Hunter, MD and Woodruff, PWR (2012) Auditory hallucinations: expectation-perception model. Medical Hypotheses 78, 802–810.Google Scholar
Nuechterlein, K and Green, M (2006) MCCB: Matrics Consensus Cognitive Battery. Los Angeles, CA: MATRICS Assessment Inc.Google Scholar
Paavilainen, P, Alho, K, Reinikainen, K, Sams, M and Näätänen, R (1991) Right hemisphere dominance of different mismatch negativities. Electroencephalography and Clinical Neurophysiology 78, 466–479.Google Scholar
Paavilainen, P, Valppu, S, Naatanen, R and Näätänen, R (2001) The additivity of the auditory feature analysis in the human brain as indexed by the mismatch negativity: 1 + 1 ≈ 2 but 1 + 1 + 1 < 3. Neuroscience Letters 301, 179–182.Google Scholar
Perez, VB, Woods, SW, Roach, BJ, Ford, JM, McGlashan, TH, Srihari, VH and Mathalon, DH (2014) Automatic auditory processing deficits in schizophrenia and clinical high-risk patients: forecasting psychosis risk with mismatch negativity. Biological Psychiatry 75, 459–469.Google Scholar
Perez, VB, Tarasenko, M, Miyakoshi, M, Pianka, ST, Makeig, SD, Braff, DL, Swerdlow, NR and Light, GA (2017) Mismatch negativity is a sensitive and predictive biomarker of perceptual learning during auditory cognitive training in schizophrenia. Neuropsychopharmacology 42, 2206–2213.Google Scholar
Rissling, AJ, Park, S-H, Young, JW, Rissling, MB, Sugar, CA, Sprock, J, Mathias, DJ, Pela, M, Sharp, RF, Braff, DL and Light, GA (2013) Demand and modality of directed attention modulate ‘pre-attentive’ sensory processes in schizophrenia patients and nonpsychiatric controls. Schizophrenia Research 146, 326–335.Google Scholar
Schmack, K, Schnack, A, Priller, J and Sterzer, P (2015) Perceptual instability in schizophrenia: probing predictive coding accounts of delusions with ambiguous stimuli. Schizophrenia Research Cognition 2, 72–77.Google Scholar
Schroger, E (1995) Processing of auditory deviants with changes in one versus two stimulus dimensions. Psychophysiology 32, 55–65.Google Scholar
Schultz, W and Dickinson, A (2000) Neuronal coding of prediction errors. Annual Review of Neuroscience 23, 473–500.Google Scholar
Shrout, PE and Fleiss, JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychological Bulletin 86, 420–428.Google Scholar
Stephan, KE, Baldeweg, T and Friston, KJ (2006) Synaptic plasticity and dysconnection in schizophrenia. Biological Psychiatry 59, 929–939.Google Scholar
Stephan, KE, Friston, KJ and Frith, CD (2009) Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bulletin 35, 509–527.Google Scholar
Takegata, R, Paavilainen, P, Naatanen, R, Winkler, I, Näätänen, R and Winkler, I (1999) Independent processing of changes in auditory single features and feature conjunctions in humans as indexed by the mismatch negativity. Neuroscience Letters 266, 109–112.Google Scholar
Thomas, ML, Green, MF, Hellemann, G, Sugar, CA, Tarasenko, M, Calkins, ME, Greenwood, TA, Gur, RE, Gur, RE, Lazzeroni, LC, Nuechterlein, KH, Radant, AD, Seidman, LJ, Shiluk, AL, Siever, LJ, Silverman, JM, Sprock, J, Stone, WS, Swerdlow, NR, Tsuang, DW, Tsuang, MT, Turetsky, BI, Braff, DL and Light, GA (2017) Modeling deficits from early auditory information processing to psychosocial functioning in schizophrenia. JAMA Psychiatry 74, 37–46.Google Scholar
Todd, J, Michie, PT, Schall, U, Karayanidis, F, Yabe, H and Näätänen, R (2008) Deviant matters: duration, frequency, and intensity deviants reveal different patterns of mismatch negativity reduction in early and late schizophrenia. Biological Psychiatry 63, 58–64.Google Scholar
Todd, J, Harms, L, Schall, U and Michie, PT (2013) Mismatch negativity: translating the potential. Frontiers in Psychiatry 4, 1–22.Google Scholar
Umbricht, D and Krljes, S (2005) Mismatch negativity in schizophrenia: a meta-analysis. Schizophrenia Research 76, 1–23.Google Scholar
Wacongne, C (2016) A predictive coding account of MMN reduction in schizophrenia. Biological Psychology 116, 68–74.Google Scholar
Wacongne, C, Changeux, J-P and Dehaene, S (2012) A neuronal model of predictive coding accounting for the mismatch negativity. Journal of Neuroscience 32, 3665–3678.Google Scholar
Winkler, I and Czigler, I (2012) Evidence from auditory and visual event-related potential (ERP) studies of deviance detection (MMN and vMMN) linking predictive coding theories and perceptual object representations. International Journal of Psychophysiology 83, 132–143.Google Scholar
Winkler, I, Reinikainen, K and Näätänen, R (1993) Event-related brain potentials reflect traces of echoic memory in humans. Perception & Psychophysics 53, 443–449.Google Scholar
Winkler, I, Cowan, N, Csépe, V, Czigler, I and Näätänen, R (1996) Interactions between transient and long-term auditory memory as reflected by the mismatch negativity. Journal of Cognitive Neuroscience 8, 403–415.Google Scholar
Wolff, C and Schröger, E (2001) Human pre-attentive auditory change-detection with single, double, and triple deviations as revealed by mismatch negativity additivity. Neuroscience Letters 311, 37–40.Google Scholar
Wynn, JK, Sugar, C, Horan, WP, Kern, R and Green, MF (2010) Mismatch negativity, social cognition, and functioning in schizophrenia patients. Biological Psychiatry 67, 940–947.Google Scholar
Supplementary material: File

McCleery supplementary material

McCleery supplementary material 1

Download McCleery supplementary material(File)
File 34 KB