A generic deviance detection principle for cortical On/Off responses, omission response, and mismatch negativity

Neural responses to sudden changes can be observed in many parts of the sensory pathways at different organizational levels. For example, deviants that violate regularity at various levels of abstraction can be observed as simple On/Off responses of individual neurons or as cumulative responses of neural populations. The cortical deviance-related responses supporting different functionalities (e.g., gap detection, chunking, etc.) seem unlikely to arise from different function-specific neural circuits, given the relatively uniform and self-similar wiring patterns across cortical areas and spatial scales. Additionally, reciprocal wiring patterns (with heterogeneous combinations of excitatory and inhibitory connections) in the cortex naturally speak in favor of a generic deviance detection principle. Based on this concept, we propose a network model consisting of reciprocally coupled neural masses as a blueprint of a universal change detector. Simulation examples reproduce properties of cortical deviance-related responses including the On/Off responses, the omitted-stimulus response (OSR), and the mismatch negativity (MMN). We propose that the emergence of change detectors relies on the involvement of disinhibition. An analysis of network connection settings further suggests a supportive effect of synaptic adaptation and a destructive effect of N-methyl-d-aspartate receptor (NMDA-r) antagonists on change detection. We conclude that the nature of cortical reciprocal wiring gives rise to a whole range of local change detectors supporting the notion of a generic deviance detection principle. Several testable predictions are provided based on the network model. Notably, we predict that the NMDA-r antagonists would generally dampen the cortical Off response, the cortical OSR, and the MMN.

[1]  E. Schröger,et al.  Omission mismatch negativity builds up late , 2010, Neuroreport.

[2]  R. Näätänen,et al.  Automatic time perception in the human brain for intervals ranging from milliseconds to seconds. , 2004, Psychophysiology.

[3]  Virginie van Wassenhove,et al.  Duration estimation entails predicting when , 2015, NeuroImage.

[4]  Simone Kurt,et al.  Quantitative analysis of neuronal response properties in primary and higher-order auditory cortical fields of awake house mice (Mus musculus) , 2014, The European journal of neuroscience.

[5]  Karl J. Friston,et al.  Brain responses in humans reveal ideal observer-like sensitivity to complex acoustic patterns , 2016, Proceedings of the National Academy of Sciences.

[6]  F. H. Lopes da Silva,et al.  Functional localization of brain sources using EEG and/or MEG data: volume conductor and source models. , 2004, Magnetic resonance imaging.

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

[8]  D. P. Phillips,et al.  Central auditory onset responses, and temporal asymmetries in auditory perception , 2002, Hearing Research.

[9]  Sibylle C. Herholz,et al.  Effects of musical training and event probabilities on encoding of complex tone patterns , 2013, BMC Neuroscience.

[10]  Erich Schröger,et al.  Regularity Extraction and Application in Dynamic Auditory Stimulus Sequences , 2007, Journal of Cognitive Neuroscience.

[11]  M. Penttonen,et al.  Auditory Cortical and Hippocampal-System Mismatch Responses to Duration Deviants in Urethane-Anesthetized Rats , 2013, PloS one.

[12]  T. Hashikawa,et al.  Temporal Integration and Duration Tuning in the Dorsal Zone of Cat Auditory Cortex , 1997, The Journal of Neuroscience.

[13]  Risto Näätänen,et al.  Mismatch negativity and behavioural discrimination in humans as a function of the magnitude of change in sound duration , 2000, Neuroscience Letters.

[14]  H. Tiitinen,et al.  Human cortical processing of auditory events over time , 2001, Neuroreport.

[15]  M. Tervaniemi,et al.  Neonatal frequency discrimination in 250–4000-Hz range: Electrophysiological evidence , 2007, Clinical Neurophysiology.

[16]  Matthias H Hennig,et al.  The Sound of Silence: Ionic Mechanisms Encoding Sound Termination , 2011, Neuron.

[17]  M. Hasselmo,et al.  NMDA-dependent modulation of CA1 local circuit inhibition , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[19]  G. Spirou,et al.  Physiological response properties of neurons in the superior paraolivary nucleus of the rat. , 2003, Journal of neurophysiology.

[20]  J. Mäkelä,et al.  Human auditory cortex is activated by omissions of auditory stimuli , 1997, Brain Research.

[21]  C. Dobel,et al.  A systematic review of the mismatch negativity as an index for auditory sensory memory: From basic research to clinical and developmental perspectives. , 2015, Psychophysiology.

[22]  Karl J. Friston,et al.  The Cumulative Effects of Predictability on Synaptic Gain in the Auditory Processing Stream , 2017, The Journal of Neuroscience.

[23]  M. Schönwiesner,et al.  Tracing the neural basis of auditory entrainment , 2016, Neuroscience.

[24]  Ling Qin,et al.  Comparison between offset and onset responses of primary auditory cortex ON-OFF neurons in awake cats. , 2007, Journal of neurophysiology.

[25]  I. Winkler,et al.  Memory prerequisites of mismatch negativity in the auditory event-related potential (ERP). , 1993, Journal of experimental psychology. Learning, memory, and cognition.

[26]  D. Javitt,et al.  Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers: implications for models of cognitive deficits in schizophrenia. , 2000, Archives of general psychiatry.

[27]  G. Karmos,et al.  Adaptive modeling of the unattended acoustic environment reflected in the mismatch negativity event-related potential , 1996, Brain Research.

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

[29]  R. Näätänen,et al.  Auditory frequency discrimination and event-related potentials. , 1985, Electroencephalography and clinical neurophysiology.

[30]  C. Escera,et al.  Deviance-Related Responses along the Auditory Hierarchy: Combined FFR, MLR and MMN Evidence , 2015, PloS one.

[31]  B. Godde,et al.  A Map of Periodicity Orthogonal to Frequency Representation in the Cat Auditory Cortex , 2009, Frontiers in integrative neuroscience.

[32]  Karin Schwab,et al.  Modeling Brain Resonance Phenomena Using a Neural Mass Model , 2011, PLoS Comput. Biol..

[33]  M. Wehr,et al.  Nonoverlapping Sets of Synapses Drive On Responses and Off Responses in Auditory Cortex , 2010, Neuron.

[34]  C. Escera,et al.  The accuracy of sound duration representation in the human brain determines the accuracy of behavioural perception , 2000, The European journal of neuroscience.

[35]  Conny Kopp-Scheinpflug,et al.  When Sound Stops: Offset Responses in the Auditory System , 2018, Trends in Neurosciences.

[36]  Sibylle C. Herholz,et al.  Looking for a pattern: An MEG study on the abstract mismatch negativity in musicians and nonmusicians , 2009, BMC Neuroscience.

[37]  Edward W. Large,et al.  A canonical model for gradient frequency neural networks , 2010 .

[38]  Christopher L Passaglia,et al.  Complex temporal response patterns with a simple retinal circuit. , 2008, Journal of neurophysiology.

[39]  A. Moossavi,et al.  Topographic comparison of MMN to simple versus pattern regularity violations: The effect of timing , 2016, Neuroscience Research.

[40]  R. Kakigi,et al.  Echoic Memory: Investigation of Its Temporal Resolution by Auditory Offset Cortical Responses , 2014, PloS one.

[41]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[42]  M. Schönwiesner,et al.  Heschl's gyrus, posterior superior temporal gyrus, and mid-ventrolateral prefrontal cortex have different roles in the detection of acoustic changes. , 2007, Journal of neurophysiology.

[43]  Laura Busse,et al.  The ERP omitted stimulus response to “no-stim” events and its implications for fast-rate event-related fMRI designs , 2003, NeuroImage.

[44]  Jean-Marc Edeline,et al.  Evoked oscillations in unit recordings from the thalamo-cortical auditory system: an aspect of temporal processing or the reflection of hyperpolarized brain states? , 2004, Acta neurobiologiae experimentalis.

[45]  R. Kakigi,et al.  Change-related responses in the human auditory cortex: an MEG study. , 2011, Psychophysiology.

[46]  Yung-Yang Lin,et al.  Memory-based mismatch response to changes in duration of auditory stimuli: An MEG study , 2010, Clinical Neurophysiology.

[47]  Tonal response patterns of primary auditory cortex neurons in alert cats , 2002, Brain Research.

[48]  R Näätänen,et al.  Effects of spectral complexity and sound duration on automatic complex-sound pitch processing in humans – a mismatch negativity study , 2000, Neuroscience Letters.

[49]  C. Escera,et al.  Activation of brain mechanisms of attention switching as a function of auditory frequency change , 2001, Neuroreport.

[50]  R. Hari,et al.  The Human Auditory Sensory Memory Trace Persists about 10 sec: Neuromagnetic Evidence , 1993, Journal of Cognitive Neuroscience.

[51]  K. Reinikainen,et al.  Do event-related potentials reveal the mechanism of the auditory sensory memory in the human brain? , 1989, Neuroscience Letters.

[52]  T H Bullock,et al.  Event-related potentials to omitted visual stimuli in a reptile. , 1994, Electroencephalography and clinical neurophysiology.

[53]  R. Burkard,et al.  Onset and offset responses from inferior colliculus and auditory cortex to paired noisebursts: inner hair cell loss , 2002, Hearing Research.

[54]  Michael J. Berry,et al.  Sophisticated temporal pattern recognition in retinal ganglion cells. , 2008, Journal of neurophysiology.

[55]  K Alho,et al.  Cerebral mechanisms underlying orienting of attention towards auditory frequency changes , 2001, Neuroreport.

[56]  K. Reinikainen,et al.  Attentive novelty detection in humans is governed by pre-attentive sensory memory , 1994, Nature.

[57]  Jufang He Corticofugal modulation on both ON and OFF responses in the nonlemniscal auditory thalamus of the guinea pig. , 2003, Journal of neurophysiology.

[58]  C. Wacongne A predictive coding account of MMN reduction in schizophrenia , 2016, Biological Psychology.

[59]  Paul Cisek,et al.  Spiking neurons that keep the rhythm , 2011, Journal of Computational Neuroscience.

[60]  Timothy D. Griffiths,et al.  Orthogonal representation of sound dimensions in the primate midbrain , 2011, Nature Neuroscience.

[61]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[62]  Na Xu,et al.  The function of offset neurons in auditory information processing , 2014 .

[63]  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.

[64]  Brice Bathellier,et al.  Temporal asymmetries in auditory coding and perception reflect multi-layered nonlinearities , 2016, Nature Communications.

[65]  Gregory Hickok,et al.  Orthogonal acoustic dimensions define auditory field maps in human cortex , 2012, Proceedings of the National Academy of Sciences.

[66]  I. Winkler,et al.  The role of attention in the formation of auditory streams , 2007, Perception & psychophysics.

[67]  Event-related potentials in an invertebrate: crayfish emit 'omitted stimulus potentials'. , 2001, The Journal of experimental biology.

[68]  R. Kakigi,et al.  Automatic auditory off‐response in humans: an MEG study , 2009, The European journal of neuroscience.

[69]  T H Bullock,et al.  Event-related potentials in the retina and optic tectum of fish. , 1990, Journal of neurophysiology.

[70]  Kuniyuki Takahashi,et al.  Auditory cortical field coding long-lasting tonal offsets in mice , 2016, Scientific Reports.

[71]  G. Recanzone Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys , 2000, Hearing Research.

[72]  R. Rübsamen,et al.  Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil , 2002, Hearing Research.

[73]  Yan Gai ON and OFF inhibition as mechanisms for forward masking in the inferior colliculus: a modeling study. , 2016, Journal of neurophysiology.

[74]  R Näätänen,et al.  The mismatch negativity as an index of temporal processing in audition , 2001, Clinical Neurophysiology.

[75]  István Ulbert,et al.  Separation of mismatch negativity and the N1 wave in the auditory cortex of the cat: a topographic study , 2001, Clinical Neurophysiology.

[76]  Andreas Spiegler,et al.  Bifurcation Analysis of Neural Mass Models , 2010 .

[77]  T. Penney,et al.  Probing interval timing with scalp-recorded electroencephalography (EEG). , 2014, Advances in experimental medicine and biology.

[78]  Christoph Kapfer,et al.  Auditory response properties in the superior paraolivary nucleus of the gerbil. , 2002, Journal of neurophysiology.

[79]  R. Kakigi,et al.  Auditory N1 as a change-related automatic response , 2011, Neuroscience Research.

[80]  R. Näätänen,et al.  Mismatch negativity to changes in a continuous tone with regularly varying frequencies. , 1994, Electroencephalography and clinical neurophysiology.

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

[82]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

[83]  Robert W. McCarley,et al.  A Pharmacological Model for Psychosis Based on N-methyl-D-aspartate Receptor Hypofunction: Molecular, Cellular, Functional and Behavioral Abnormalities , 2006, Biological Psychiatry.

[84]  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.

[85]  C. Li,et al.  Engaging and disengaging recurrent inhibition coincides with sensing and unsensing of a sensory stimulus , 2017, Nature Communications.

[86]  T H Bullock,et al.  Dynamic properties of human visual evoked and omitted stimulus potentials. , 1994, Electroencephalography and clinical neurophysiology.

[87]  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..

[88]  Chun-Yu Tse,et al.  Preattentive timing of empty intervals is from marker offset to onset. , 2006, Psychophysiology.

[89]  C. Schroeder,et al.  Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Michael J. Berry,et al.  Detection and prediction of periodic patterns by the retina , 2007, Nature Neuroscience.

[91]  P. Paavilainen The mismatch-negativity (MMN) component of the auditory event-related potential to violations of abstract regularities: a review. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[93]  A. Magnusson,et al.  Sound Rhythms Are Encoded by Postinhibitory Rebound Spiking in the Superior Paraolivary Nucleus , 2011, The Journal of Neuroscience.

[94]  Yung-Yang Lin,et al.  Cortico-cortical phase synchrony in auditory mismatch processing , 2010, Biological Psychology.

[95]  I. Winkler,et al.  Mismatch negativity to pitch change: varied stimulus proportions in controlling effects of neural refractoriness on human auditory event-related brain potentials , 2003, Neuroscience Letters.

[96]  Pejman Sehatpour,et al.  Neural mechanisms of mismatch negativity (MMN) dysfunction in schizophrenia , 2016, Molecular Psychiatry.

[97]  I. Volkov,et al.  Formation of spike response to sound tones in cat auditory cortex neurons: Interaction of excitatory and inhibitory effects , 1991, Neuroscience.

[98]  Warren H Meck,et al.  Timing in the baby brain. , 2004, Brain research. Cognitive brain research.

[99]  Sibylle C. Herholz,et al.  Processing of Complex Auditory Patterns in Musicians and Nonmusicians , 2011, PloS one.

[100]  Jean Vroomen,et al.  Predictive coding of visual–auditory and motor-auditory events: An electrophysiological study , 2015, Brain Research.

[101]  P. Deltenre,et al.  Mismatch Negativity (MMN) evoked by sound duration contrasts: An unexpected major effect of deviance direction on amplitudes , 2009, Clinical Neurophysiology.

[102]  R. Kanzaki,et al.  Cortical Mapping of Mismatch Negativity with Deviance Detection Property in Rat , 2013, PloS one.

[103]  T H Bullock,et al.  Dynamics of event-related potentials to trains of light and dark flashes: responses to missing and extra stimuli in elasmobranch fish. , 1994, Electroencephalography and clinical neurophysiology.

[104]  Daniel C. Javitt,et al.  Auditory dysfunction in schizophrenia: integrating clinical and basic features , 2015, Nature Reviews Neuroscience.

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

[106]  R. Ilmoniemi,et al.  Language-specific phoneme representations revealed by electric and magnetic brain responses , 1997, Nature.

[107]  R. Näätänen,et al.  The mismatch negativity (MMN) in basic research of central auditory processing: A review , 2007, Clinical Neurophysiology.

[108]  T. Bullock,et al.  Human Auditory Fast and Slow Omitted Stimulus Potentials and Steady-State Responses , 2000, The International journal of neuroscience.

[109]  M. H. Hofmann,et al.  Interval-specific event related potentials to omitted stimuli in the electrosensory pathway in elasmobranchs: an elementary form of expectation , 1993, Journal of Comparative Physiology A.

[110]  Ben H. Jansen,et al.  A neurophysiologically-based mathematical model of flash visual evoked potentials , 2004, Biological Cybernetics.

[111]  I. Nelken,et al.  Sensitivity to Complex Statistical Regularities in Rat Auditory Cortex , 2012, Neuron.

[112]  Kimitaka Kaga,et al.  Cortical mapping of auditory-evoked offset responses in rats , 2004, Neuroreport.

[113]  H. Tiitinen,et al.  Computational modelling suggests that temporal integration results from synaptic adaptation in auditory cortex , 2015, The European journal of neuroscience.

[114]  Maria Chait,et al.  Sensitivity to the temporal structure of rapid sound sequences — An MEG study , 2015, NeuroImage.

[115]  Risto Näätänen,et al.  Frequency discrimination at different frequency levels as indexed by electrophysiological and behavioral measures. , 2004, Brain research. Cognitive brain research.

[116]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[117]  Angela D. Friederici,et al.  Early Parallel Processing of Auditory Word and Voice Information , 2002, NeuroImage.