Repetition suppression and repetition enhancement underlie auditory memory-trace formation in the human brain: an MEG study

The formation of echoic memory traces has traditionally been inferred from the enhanced responses to its deviations. The mismatch negativity (MMN), an auditory event-related potential (ERP) elicited between 100 and 250ms after sound deviation is an indirect index of regularity encoding that reflects a memory-based comparison process. Recently, repetition positivity (RP) has been described as a candidate ERP correlate of direct memory trace formation. RP consists of repetition suppression and enhancement effects occurring in different auditory components between 50 and 250ms after sound onset. However, the neuronal generators engaged in the encoding of repeated stimulus features have received little interest. This study intends to investigate the neuronal sources underlying the formation and strengthening of new memory traces by employing a roving-standard paradigm, where trains of different frequencies and different lengths are presented randomly. Source generators of repetition enhanced (RE) and suppressed (RS) activity were modeled using magnetoencephalography (MEG) in healthy subjects. Our results show that, in line with RP findings, N1m (~95-150ms) activity is suppressed with stimulus repetition. In addition, we observed the emergence of a sustained field (~230-270ms) that showed RE. Source analysis revealed neuronal generators of RS and RE located in both auditory and non-auditory areas, like the medial parietal cortex and frontal areas. The different timing and location of neural generators involved in RS and RE points to the existence of functionally separated mechanisms devoted to acoustic memory-trace formation in different auditory processing stages of the human brain.

[1]  T. Baldeweg,et al.  Mismatch negativity potentials and cognitive impairment in schizophrenia , 2004, Schizophrenia Research.

[2]  Linda V. Heinemann,et al.  Auditory repetition enhancement at short interstimulus intervals for frequency-modulated tones , 2011, Brain Research.

[3]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[4]  A. Mouraux,et al.  The Enhancement of the N1 Wave Elicited by Sensory Stimuli Presented at Very Short Inter-Stimulus Intervals Is a General Feature across Sensory Systems , 2008, PloS one.

[5]  S. Grimm,et al.  Ultrafast tracking of sound location changes as revealed by human auditory evoked potentials , 2012, Biological Psychology.

[6]  Jordi Costa-Faidella,et al.  Multiple time scales of adaptation in the auditory system as revealed by human evoked potentials. , 2011, Psychophysiology.

[7]  Antoine J. Shahin,et al.  Sensitivity of EEG and MEG to the N1 and P2 Auditory Evoked Responses Modulated by Spectral Complexity of Sounds , 2007, Brain Topography.

[8]  S. Grimm,et al.  Detection of Simple and Pattern Regularity Violations Occurs at Different Levels of the Auditory Hierarchy , 2012, PloS one.

[9]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[10]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  Ravi S. Menon,et al.  The effects of visual object priming on brain activation before and after recognition , 2000, Current Biology.

[12]  Linda V. Heinemann,et al.  Repetition Enhancement for Frequency-Modulated but Not Unmodulated Sounds: A Human MEG Study , 2010, PloS one.

[13]  Josep Marco-Pallarés,et al.  Functional neural dynamics underlying auditory event-related N1 and N1 suppression response , 2007, NeuroImage.

[14]  Daniel L. Schacter,et al.  Specificity of priming: a cognitive neuroscience perspective , 2004, Nature Reviews Neuroscience.

[15]  Nash N. Boutros,et al.  Mapping Repetition Suppression of the N100 Evoked Response to the Human Cerebral Cortex , 2011, Biological Psychiatry.

[16]  S. Grimm,et al.  Deviance Detection Based on Regularity Encoding Along the Auditory Hierarchy: Electrophysiological Evidence in Humans , 2013, Brain Topography.

[17]  Julia M. Stephen,et al.  Modulatory role of the prefrontal generator within the auditory M50 network , 2014, NeuroImage.

[18]  I. Winkler,et al.  ‘Primitive intelligence’ in the auditory cortex , 2001, Trends in Neurosciences.

[19]  Amy Poremba,et al.  Neural correlates of short-term memory in primate auditory cortex , 2014, Front. Neurosci..

[20]  Amy Poremba,et al.  Neural correlates of auditory recognition memory in the primate dorsal temporal pole. , 2014, Journal of neurophysiology.

[21]  P. Michie,et al.  Event-related potentials reveal modelling of auditory repetition in the brain. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  Hubert Preissl,et al.  Modulations of neural activity in auditory streaming caused by spectral and temporal alternation in subsequent stimuli: a magnetoencephalographic study , 2012, BMC Neuroscience.

[23]  M. Malmierca,et al.  Stimulus-specific adaptation in the inferior colliculus of the mouse: anesthesia and spontaneous activity effects , 2015, Brain Structure and Function.

[24]  D. Javitt,et al.  Impaired mismatch negativity (MMN) generation in schizophrenia as a function of stimulus deviance, probability, and interstimulus/interdeviant interval. , 1998, Electroencephalography and clinical neurophysiology.

[25]  T. Baldeweg,et al.  Differential changes in frontal and sub-temporal components of mismatch negativity. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  N. Cowan On short and long auditory stores. , 1984, Psychological bulletin.

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

[28]  Anders M. Dale,et al.  Right hemisphere has the last laugh: neural dynamics of joke appreciation , 2010, Cognitive, affective & behavioral neuroscience.

[29]  S. Kochen,et al.  Expectation and Attention in Hierarchical Auditory Prediction , 2013, The Journal of Neuroscience.

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

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

[32]  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.

[33]  M Scherg,et al.  Is frontal lobe involved in the generation of auditory evoked P50? , 2001, Neuroreport.

[34]  S. Grimm,et al.  Simple and complex acoustic regularities are encoded at different levels of the auditory hierarchy , 2013, The European journal of neuroscience.

[35]  D. Vernon,et al.  Event-Related Brain Potential Correlates of Human Auditory Sensory Memory-Trace Formation , 2005, The Journal of Neuroscience.

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

[37]  Blaise Yvert,et al.  Localization of human supratemporal auditory areas from intracerebral auditory evoked potentials using distributed source models , 2005, NeuroImage.

[38]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[39]  A. Zador,et al.  Auditory cortex mediates the perceptual effects of acoustic temporal expectation , 2010, Nature Neuroscience.

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

[41]  N. Crone,et al.  Adaptation of high-gamma responses in human auditory association cortex. , 2014, Journal of neurophysiology.

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

[43]  M. Malmierca,et al.  The auditory novelty system: an attempt to integrate human and animal research. , 2014, Psychophysiology.

[44]  R. Näätänen Attention and brain function , 1992 .

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

[46]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[48]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[49]  R. Ilmoniemi,et al.  Combined mapping of human auditory EEG and MEG responses. , 1998, Electroencephalography and clinical neurophysiology.

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

[51]  P. Hagoort,et al.  The suppression of repetition enhancement: A review of fMRI studies , 2013, Neuropsychologia.

[52]  Péter Szigetvári,et al.  What and When? , 2019, Inauguration and Liturgical Kingship in the Long Twelfth Century.

[53]  M. Malmierca,et al.  Effect of Auditory Cortex Deactivation on Stimulus-Specific Adaptation in the Medial Geniculate Body , 2011, The Journal of Neuroscience.

[54]  B Opitz,et al.  Sensory and cognitive mechanisms for preattentive change detection in auditory cortex , 2005, The European journal of neuroscience.

[55]  G. A. Miller,et al.  Predicting EEG responses using MEG sources in superior temporal gyrus reveals source asynchrony in patients with schizophrenia , 2003, Clinical Neurophysiology.

[56]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[57]  Jordi Costa-Faidella,et al.  Interactions between “What” and “When” in the Auditory System: Temporal Predictability Enhances Repetition Suppression , 2011, The Journal of Neuroscience.

[58]  T. Baldeweg ERP Repetition Effects and Mismatch Negativity Generation A Predictive Coding Perspective , 2007 .

[59]  O Bertrand,et al.  Multiple supratemporal sources of magnetic and electric auditory evoked middle latency components in humans. , 2001, Cerebral cortex.

[60]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[61]  R. Hari,et al.  Interstimulus interval dependence of the auditory vertex response and its magnetic counterpart: implications for their neural generation. , 1982, Electroencephalography and clinical neurophysiology.

[62]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Risto Näätänen,et al.  Electric brain response to sound repetition in humans: an index of long-term-memory – trace formation? , 2002, Neuroscience Letters.

[64]  A. Dale,et al.  Human posterior auditory cortex gates novel sounds to consciousness. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[66]  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.

[67]  J. Snyder,et al.  Effects of context on auditory stream segregation. , 2008, Journal of experimental psychology. Human perception and performance.

[68]  R. Todd Constable,et al.  Comparator and non-comparator mechanisms of change detection in the context of speech — An ERP study , 2009, NeuroImage.

[69]  Erich Schröger,et al.  Auditory distraction by duration and location deviants: a behavioral and event-related potential study. , 2003, Brain research. Cognitive brain research.

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

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

[72]  I. Nelken,et al.  Stimulus-Specific Adaptation in the Auditory Thalamus of the Anesthetized Rat , 2010, PloS one.

[73]  Jordi Costa-Faidella,et al.  Early change detection in humans as revealed by auditory brainstem and middle‐latency evoked potentials , 2010, The European journal of neuroscience.

[74]  F. Perrin,et al.  Brain generators implicated in the processing of auditory stimulus deviance: a topographic event-related potential study. , 1990, Psychophysiology.

[75]  T. Baldeweg Repetition effects to sounds: evidence for predictive coding in the auditory system , 2006, Trends in Cognitive Sciences.

[76]  Eric Halgren,et al.  Spatiotemporal neural dynamics of word understanding in 12- to 18-month-old-infants. , 2011, Cerebral cortex.

[77]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[78]  S. Grimm,et al.  Encoding of nested levels of acoustic regularity in hierarchically organized areas of the human auditory cortex , 2014, Human brain mapping.

[79]  R. Näätänen The Mismatch Negativity: A Powerful Tool for Cognitive Neuroscience , 1995, Ear and hearing.

[80]  Uwe Pietrzyk,et al.  Integration of Amplitude and Phase Statistics for Complete Artifact Removal in Independent Components of Neuromagnetic Recordings , 2008, IEEE Transactions on Biomedical Engineering.

[81]  I. Nelken,et al.  Multiple Time Scales of Adaptation in Auditory Cortex Neurons , 2004, The Journal of Neuroscience.

[82]  J. L. Cantero,et al.  The time course of neural changes underlying auditory perceptual learning. , 2002, Learning & memory.

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

[84]  W. Ritter,et al.  Storage of information in transient auditory memory. , 1996, Brain research. Cognitive brain research.

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

[86]  M. Malmierca,et al.  Stimulus-specific adaptation and deviance detection in the inferior colliculus , 2013, Front. Neural Circuits.

[87]  L. McEvoy,et al.  Determinants of the auditory mismatch response. , 1993, Electroencephalography and clinical neurophysiology.

[88]  Minna Huotilainen,et al.  Is there a direct neural correlate for memory-trace formation in audition? , 2007, Neuroreport.

[89]  Karl J. Friston,et al.  Repetition suppression and plasticity in the human brain , 2009, NeuroImage.

[90]  S. Grimm,et al.  Two sequential processes of change detection in hierarchically ordered areas of the human auditory cortex. , 2014, Cerebral cortex.

[91]  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.

[92]  Oleg Korzyukov,et al.  Generators of the intracranial P50 response in auditory sensory gating , 2007, NeuroImage.

[93]  Stephen Mumford,et al.  Effects of context , 2011, Inf. Knowl. Syst. Manag..

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

[95]  R. Näätänen,et al.  Short-term habituation and dishabituation of the mismatch negativity of the ERP. , 1984, Psychophysiology.

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

[97]  C. Rennie,et al.  Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[98]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[99]  J. Snyder,et al.  Effects of prior stimulus and prior perception on neural correlates of auditory stream segregation. , 2009, Psychophysiology.

[100]  M. Malmierca,et al.  Novelty detector neurons in the mammalian auditory midbrain , 2005, The European journal of neuroscience.

[101]  R. Hari,et al.  Evoked responses of human auditory cortex may be enhanced by preceding stimuli. , 1989, Electroencephalography and clinical neurophysiology.

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

[103]  K. Stephan,et al.  Nicotinic modulation of human auditory sensory memory: Evidence from mismatch negativity potentials. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[105]  Ulrich Schall,et al.  Dorsolateral prefrontal cortex activation during automatic auditory duration-mismatch processing in humans: a positron emission tomography study , 2001, Neuroscience Letters.

[106]  Jordi Costa-Faidella,et al.  Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain. , 2011, Psychophysiology.