Test–retest reliability of the magnetic mismatch negativity response to sound duration and omission deviants

&NA; Mismatch negativity (MMN) is a neurophysiological measure of auditory novelty detection that could serve as a translational biomarker of psychiatric disorders, such as schizophrenia. However, the replicability of its magnetoencephalographic (MEG) counterpart (MMNm) has been insufficiently addressed. In the current study, test–retest reliability of the MMNm response to both duration and omission deviants was evaluated over two MEG sessions in 16 healthy adults. MMNm amplitudes and latencies were obtained at both sensor‐ and source‐level using a cortically‐constrained minimum‐norm approach. Intraclass correlations (ICC) were derived to assess stability of MEG responses over time. In addition, signal‐to‐noise ratios (SNR) and within‐subject statistics were obtained in order to determine MMNm detectability in individual participants. ICC revealed robust values at both sensor‐ and source‐level for both duration and omission MMNm amplitudes (ICC = 0.81–0.90), in particular in the right hemisphere, while moderate to strong values were obtained for duration MMNm and omission MMNm peak latencies (ICC = 0.74–0.88). Duration MMNm was robustly identified in individual participants with high SNR, whereas omission MMNm responses were only observed in half of the participants. Our data indicate that MMNm to unexpected duration changes and omitted sounds are highly reproducible, providing support for the use of MEG‐parameters in basic and clinical research.

[1]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[2]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[3]  S. Dehaene,et al.  Evidence for a hierarchy of predictions and prediction errors in human cortex , 2011, Proceedings of the National Academy of Sciences.

[4]  S. Dehaene,et al.  Neural signature of the conscious processing of auditory regularities , 2009, Proceedings of the National Academy of Sciences.

[5]  John J. Foxe,et al.  The neural circuitry of pre-attentive auditory change-detection: an fMRI study of pitch and duration mismatch negativity generators. , 2005, Cerebral cortex.

[6]  Wolfgang Grodd,et al.  Mismatch responses to randomized gradient switching noise as reflected by fMRI and whole‐head magnetoencephalography , 2002, Human brain mapping.

[7]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[8]  Karl J. Friston,et al.  Repetition suppression and its contextual determinants in predictive coding , 2016, Cortex.

[9]  I. Winkler,et al.  Mismatch negativity , 1998, Clinical Neurophysiology.

[10]  R. Näätänen,et al.  The mismatch negativity (MMN): towards the optimal paradigm , 2004, Clinical Neurophysiology.

[11]  K. Alho,et al.  Separate Time Behaviors of the Temporal and Frontal Mismatch Negativity Sources , 2000, NeuroImage.

[12]  Timm Rosburg,et al.  Hippocampal event-related potentials to tone duration deviance in a passive oddball paradigm in humans , 2007, NeuroImage.

[13]  David Cucurell,et al.  On the number of trials needed for a stable feedback-related negativity. , 2011, Psychophysiology.

[14]  Gregory A Miller,et al.  Improved test-retest reliability of 50-ms paired-click auditory gating using magnetoencephalography source modeling. , 2007, Psychophysiology.

[15]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[16]  R. Näätänen,et al.  Variability and replicability of the mismatch negativity. , 1995, Electroencephalography and clinical neurophysiology.

[17]  Erich Schröger,et al.  I know what is missing here: electrophysiological prediction error signals elicited by omissions of predicted ”what” but not ”when” , 2013, Front. Hum. Neurosci..

[18]  Michael Wagner,et al.  Prediction of Psychosis by Mismatch Negativity , 2011, Biological Psychiatry.

[19]  J. Changeux,et al.  A Neuronal Model of Predictive Coding Accounting for the Mismatch Negativity , 2012, The Journal of Neuroscience.

[20]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[21]  Joachim Gross,et al.  MEG—measured auditory steady-state oscillations show high test–retest reliability: A sensor and source-space analysis , 2015, NeuroImage.

[22]  Erich Schröger,et al.  Prefrontal cortex involvement in preattentive auditory deviance detection: neuroimaging and electrophysiological evidence , 2003, NeuroImage.

[23]  Jean-Marie Annoni,et al.  Experience-based Auditory Predictions Modulate Brain Activity to Silence as Do Real Sounds , 2015, Journal of Cognitive Neuroscience.

[24]  Klaus Scheffler,et al.  Temporal integration of sequential auditory events: silent period in sound pattern activates human planum temporale , 2003, NeuroImage.

[25]  R. Näätänen,et al.  Mismatch negativity (MMN) deficiency: a break-through biomarker in predicting psychosis onset. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[27]  H. Volz,et al.  Impaired sensory processing in male patients with schizophrenia—a magnetoencephalographic study of auditory mismatch detection , 1999, Schizophrenia Research.

[28]  R. Ilmoniemi,et al.  Test–retest reliability of mismatch negativity for duration, frequency and intensity changes , 1999, Clinical Neurophysiology.

[29]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

[30]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[31]  Joachim Gross,et al.  MEG sensor and source measures of visually induced gamma-band oscillations are highly reliable , 2016, NeuroImage.

[32]  M Huotilainen,et al.  The mismatch negativity for duration decrement of auditory stimuli in healthy subjects. , 1998, Electroencephalography and clinical neurophysiology.

[33]  Catherine A. Sugar,et al.  Characterization of Neurophysiologic and Neurocognitive Biomarkers for Use in Genomic and Clinical Outcome Studies of Schizophrenia , 2012, PloS one.

[34]  E. Schröger,et al.  Two separate mechanisms underlie auditory change detection and involuntary control of attention , 2006, Brain Research.

[35]  Norbert Kathmann,et al.  Stability of the mismatch negativity under different stimulus and attention conditions , 1999, Clinical Neurophysiology.

[36]  D. Braff,et al.  Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. , 2005, Archives of general psychiatry.

[37]  H. Yabe,et al.  Deviant Matters: Duration, Frequency, and Intensity Deviants Reveal Different Patterns of Mismatch Negativity Reduction in Early and Late Schizophrenia , 2008, Biological Psychiatry.

[38]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[39]  C. Klein,et al.  Inter-individual and intra-individual variability of the N2 component: On reliability and signal-to-noise ratio , 2013, Brain and Cognition.

[40]  E. Schröger,et al.  Measuring duration mismatch negativity , 2003, Clinical Neurophysiology.

[41]  Karl J. Friston,et al.  The mismatch negativity: A review of underlying mechanisms , 2009, Clinical Neurophysiology.

[42]  K. Kasai,et al.  Auditory mismatch negativity and P3a in response to duration and frequency changes in the early stages of psychosis , 2013, Schizophrenia Research.

[43]  ChrisD . Frith,et al.  Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia , 2009, Nature Reviews Neuroscience.

[44]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[45]  Karl J. Friston,et al.  The Computational Anatomy of Psychosis , 2013, Front. Psychiatry.

[46]  Anders M. Dale,et al.  Dynamic Statistical Parametric Neurotechnique Mapping: Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000 .

[47]  R. Näätänen,et al.  The mismatch negativity (MMN) – A unique window to disturbed central auditory processing in ageing and different clinical conditions , 2012, Clinical Neurophysiology.

[48]  I. Winkler,et al.  I Heard That Coming: Event-Related Potential Evidence for Stimulus-Driven Prediction in the Auditory System , 2009, The Journal of Neuroscience.

[49]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[50]  Norbert Kathmann,et al.  Dipole Localization and Test-Retest Reliability of Frequency and Duration Mismatch Negativity Generator Processes , 2004, Brain Topography.

[51]  Risto Näätänen,et al.  The Mismatch Negativity (MMN) , 2011 .

[52]  Karl J. Friston,et al.  The functional anatomy of the MMN: A DCM study of the roving paradigm , 2008, NeuroImage.

[53]  D. Bishop,et al.  Measurement of mismatch negativity in individuals: A study using single-trial analysis , 2010, Psychophysiology.

[54]  D. Salisbury,et al.  Abnormal Complex Auditory Pattern Analysis in Schizophrenia Reflected in an Absent Missing Stimulus Mismatch Negativity , 2016, Brain Topography.

[55]  Erich Schröger,et al.  Auditory distraction: event-related potential and behavioral indices , 2000, Clinical Neurophysiology.

[56]  H. Yabe,et al.  Temporal window of integration revealed by MMN to sound omission , 1997, Neuroreport.

[57]  Karl J. Friston,et al.  A Neurocomputational Model of the Mismatch Negativity , 2013, PLoS Comput. Biol..

[58]  H. Tiitinen,et al.  Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. , 2010, Psychophysiology.

[59]  Teemu Rinne,et al.  Superior temporal and inferior frontal cortices are activated by infrequent sound duration decrements: an fMRI study , 2005, NeuroImage.

[60]  D. Umbricht,et al.  Mismatch negativity in schizophrenia: a meta-analysis , 2005, Schizophrenia Research.

[61]  Risto Näätänen,et al.  Central auditory dysfunction in schizophrenia as revealed by the mismatch negativity (MMN) and its magnetic equivalent MMNm: a review. , 2009, The international journal of neuropsychopharmacology.

[62]  W. Roth,et al.  ERPs for infrequent omissions and inclusions of stimulus elements. , 1994, Psychophysiology.

[63]  R. Näätänen,et al.  Temporal integration of auditory information in sensory memory as reflected by the mismatch negativity , 1994, Biological Psychology.

[64]  D. Salisbury Finding the missing stimulus mismatch negativity (MMN): emitted MMN to violations of an auditory gestalt. , 2012, Psychophysiology.

[65]  R. Näätänen,et al.  Mismatch negativity is a breakthrough biomarker for understanding and treating psychotic disorders , 2013, Proceedings of the National Academy of Sciences.

[66]  R. Ilmoniemi,et al.  Temporal window of integration of auditory information in the human brain. , 1998, Psychophysiology.

[67]  Thomas R Knösche,et al.  Tangential derivative mapping of axial MEG applied to event-related desynchronization research , 2000, Clinical Neurophysiology.

[68]  E. Schröger,et al.  Attention and prediction in human audition: a lesson from cognitive psychophysiology , 2015, The European journal of neuroscience.

[69]  I. Winkler,et al.  Memory-based or afferent processes in mismatch negativity (MMN): a review of the evidence. , 2005, Psychophysiology.

[70]  R. Henson,et al.  Silent Expectations: Dynamic Causal Modeling of Cortical Prediction and Attention to Sounds That Weren't , 2016, The Journal of Neuroscience.

[71]  Risto Näätänen,et al.  Test–retest stability of the magnetic mismatch response (MMNm) , 2005, Clinical Neurophysiology.

[72]  I. Winkler,et al.  The concept of auditory stimulus representation in cognitive neuroscience. , 1999, Psychological bulletin.

[73]  Robin M. Murray,et al.  Heritability and Reliability of P300, P50 and Duration Mismatch Negativity , 2006, Behavior genetics.