Theta EEG oscillatory activity and auditory change detection

The mismatch negativity is an electrophysiological marker of auditory change detection in the event-related brain potential and has been proposed to reflect an automatic comparison process between an incoming stimulus and the representation of prior items in a sequence. There is evidence for two main functional subcomponents comprising the MMN, generated by temporal and frontal brain areas, respectively. Using data obtained in an MMN paradigm, we performed time-frequency analysis to reveal the changes in oscillatory neural activity in the theta band. The results suggest that the frontal component of the MMN is brought about by an increase in theta power for the deviant trials and, possibly, by an additional contribution of theta phase alignment. By contrast, the temporal component of the MMN, best seen in recordings from mastoid electrodes, is generated by phase resetting of theta rhythm with no concomitant power modulation. Thus, frontal and temporal MMN components do not only differ with regard to their functional significance but also appear to be generated by distinct neurophysiological mechanisms.

[1]  R. Näätänen,et al.  Human auditory-cortex mechanisms of preattentive sound discrimination , 2000, Neuroscience Letters.

[2]  Ankoor S. Shah,et al.  Neural dynamics and the fundamental mechanisms of event-related brain potentials. , 2004, Cerebral cortex.

[3]  Naoko Shinozaki,et al.  The effect of deviant stimulus probability on the human mismatch process , 2000, Neuroreport.

[4]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[5]  B. MCA. SAVERS,et al.  The Mechanism of Auditory Evoked EEG Responses , 1974, Nature.

[6]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[7]  T. Sejnowski,et al.  Electroencephalographic Brain Dynamics Following Manually Responded Visual Targets , 2004, PLoS biology.

[8]  Josep Marco-Pallarés,et al.  Combined ICA-LORETA analysis of mismatch negativity , 2005, NeuroImage.

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

[10]  C. Elger,et al.  Subdural recordings of the mismatch negativity (MMN) in patients with focal epilepsy. , 2005, Brain : a journal of neurology.

[11]  John O'Keefe,et al.  Independent rate and temporal coding in hippocampal pyramidal cells , 2003, Nature.

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

[13]  Gregory McCarthy,et al.  Graded Visual Attention Modulates Brain Responses Evoked by Task-irrelevant Auditory Pitch Changes , 2005, Journal of Cognitive Neuroscience.

[14]  Karl J. Friston,et al.  Modelling event-related responses in the brain , 2005, NeuroImage.

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

[16]  R. Ilmoniemi,et al.  Responses of the primary auditory cortex to pitch changes in a sequence of tone pips: Neuromagnetic recordings in man , 1984, Neuroscience Letters.

[17]  I. Winkler,et al.  Dynamic sensory updating in the auditory system. , 2001, Brain research. Cognitive brain research.

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

[19]  Simon Hanslmayr,et al.  Distinguishing the evoked response from phase reset: A comment to Mäkinen et al. , 2006, NeuroImage.

[20]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[21]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[22]  B. Givens.  Stimulus‐evoked resetting of the dentate theta rhythm: relation to working memory , 1996, Neuroreport.

[23]  J. Pernier,et al.  Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. , 1997, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  S. Makeig,et al.  Mining event-related brain dynamics , 2004, Trends in Cognitive Sciences.

[25]  K. Alho.  Cerebral Generators of Mismatch Negativity (MMN) and Its Magnetic Counterpart (MMNm) Elicited by Sound Changes , 1995, Ear and hearing.

[26]  Simon Hanslmayr,et al.  Alpha phase reset contributes to the generation of ERPs. , 2006, Cerebral cortex.

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

[28]  J. Yordanova,et al.  Developmental changes in the theta response system: a single-sweep analysis , 1997 .

[29]  R. Näätänen,et al.  Early selective-attention effects on the evoked potential: A critical review and reinterpretation , 1979, Biological Psychology.

[30]  R. Näätänen,et al.  Mismatch negativity subcomponents and ethyl alcohol , 1996, Biological Psychology.

[31]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[32]  György Buzsáki,et al.  Synaptic plasticity and self-organization in the hippocampus , 2005, Nature Neuroscience.

[33]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[34]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[35]  W. R. Adey,et al.  Application of phase detection and averaging techniques in computer analysis of EEG records in the cat. , 1963, Experimental neurology.

[36]  Winfried B. Müller,et al.  Cortical Activation to Auditory Mismatch Elicited by Frequency Deviant and Complex Novel Sounds: A PET Study , 2002, NeuroImage.

[37]  W. Klimesch,et al.  Alpha phase synchronization predicts P1 and N1 latency and amplitude size. , 2005, Cerebral cortex.

[38]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

[39]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

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

[41]  R. McCarley,et al.  Neural synchrony indexes disordered perception and cognition in schizophrenia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Ilmoniemi,et al.  Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings. , 1998, Psychophysiology.

[43]  Josep Marco-Pallarés,et al.  Modulation of spectral power and of phase resetting of EEG contributes differentially to the generation of auditory event-related potentials , 2006, NeuroImage.

[44]  Clay B. Holroyd,et al.  Detection of synchronized oscillations in the electroencephalogram: an evaluation of methods. , 2004, Psychophysiology.

[45]  M. Brandt,et al.  Pre-stimulus spectral EEG patterns and the visual evoked response. , 1991, Electroencephalography and clinical neurophysiology.

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

[47]  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.

[48]  J. Karhu,et al.  Impaired temporal lobe processing of preattentive auditory discrimination in schizophrenia. , 2002, Schizophrenia bulletin.

[49]  R. Näätänen,et al.  Intermodal selective attention. II. Effects of attentional load on processing of auditory and visual stimuli in central space. , 1992, Electroencephalography and clinical neurophysiology.

[50]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[51]  E. Basar.  Brain Function and Oscillations , 1998 .

[52]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

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

[54]  T. Baldeweg,et al.  Impairment in frontal but not temporal components of mismatch negativity in schizophrenia. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  S. Makeig.  Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. , 1993, Electroencephalography and clinical neurophysiology.

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

[57]  T. Picton,et al.  Mismatch Negativity: Different Water in the Same River , 2000, Audiology and Neurotology.

[58]  L. Deouell,et al.  Mismatch negativity in dichotic listening: evidence for interhemispheric differences and multiple generators. , 1998, Psychophysiology.

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

[60]  James M Kilner,et al.  Event-related brain dynamics , 2002, Trends in Neurosciences.

[61]  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.

[62]  S. Schiff,et al.  Interplay of Electroencephalogram Phase and Auditory-Evoked Neural Activity , 2003, The Journal of Neuroscience.

[63]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[64]  Risto N t nen.  Attention and brain function , 1992 .

[65]  H. Heinze,et al.  The oscillatory dynamics of recognition memory and its relationship to event-related responses. , 2005, Cerebral cortex.

[66]  M. Kahana,et al.  Reset of human neocortical oscillations during a working memory task , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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