Mapping repetition suppression of the P50 evoked response to the human cerebral cortex

OBJECTIVE The cerebral network subserving repetition suppression (RS) of the P50 auditory evoked response as observed using paired-identical-stimulus (S1-S2) paradigms is not well-described. METHODS We analyzed S1-S2 data from electrodes placed on the cortices of 64 epilepsy patients. We identified regions with maximal amplitude responses to S1 (i.e., stimulus registration), regions with maximal suppression of responses to S2 relative to S1 (i.e., RS), and regions with no or minimal RS 30-80 ms post stimulation. RESULTS Several temporal, parietal and cingulate area regions were shown to have significant initial registration activity (i.e., strong P50 response to S1). Moreover, prefrontal, cingulate, and parietal lobe regions not previously proposed to be part of the P50 habituation neural circuitry were found to exhibit significant RS. CONCLUSIONS The data suggest that the neural network underlying the initial phases of the RS process may include regions not previously thought to be involved like the parietal and cingulate cortexes. In addition, a significant role for the frontal lobe in mediating this function is supported. SIGNIFICANCE A number of regions of interest are identified through invasive recording that will allow further probing of the RS function using less invasive technology.

[1]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[2]  M. Buchsbaum.  The middle evoked response components and schizophrenia. , 1977, Schizophrenia bulletin.

[3]  K. Walton,et al.  Magnetic sources of the M50 response are localized to frontal cortex , 2008, Clinical Neurophysiology.

[4]  C. E. Elger,et al.  Subdural and depth electrodes in the presurgical evaluation of epilepsy , 2005, Acta Neurochirurgica.

[5]  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.

[6]  R. Hales,et al.  J Neuropsychiatry Clin Neurosci , 1992 .

[7]  H. C. Cromwell,et al.  Inhibitory Gating of Single Unit Activity in Amygdala: Effects of Ketamine, Haloperidol, or Nicotine , 2007, Biological Psychiatry.

[8]  K. Moxon,et al.  Sensory gating in the human hippocampal and rhinal regions: Regional differences , 2008, Hippocampus.

[9]  N. Boutros,et al.  Relevance of attention in auditory sensory gating paradigms in schizophrenia A pilot study. , 2011, Journal of psychophysiology.

[10]  Oleg Korzyukov,et al.  Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients , 2004, Psychiatry Research.

[11]  R Freedman,et al.  Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Human recordings, computer simulation, and an animal model. , 1996, Archives of general psychiatry.

[12]  Nash N. Boutros,et al.  Evidence for a frontal cortex role in both auditory and somatosensory habituation: A MEG study , 2008, NeuroImage.

[13]  Jürgen Gallinat,et al.  Test-retest reliability of P50, N100 and P200 auditory sensory gating in healthy subjects. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  I. Tendolkar,et al.  Sensory Gating in Schizophrenia: P50 and N100 Gating in Antipsychotic-Free Subjects at Risk, First-Episode, and Chronic Patients , 2008, Biological Psychiatry.

[16]  Karen A. Moxon,et al.  Inhibitory control of sensory gating in a computer model of the CA3 region of the hippocampus , 2003, Biological Cybernetics.

[17]  Mingxiong Huang,et al.  Distinct M50 and M100 auditory gating deficits in schizophrenia. , 2005, Psychophysiology.

[18]  E. Eisenstein,et al.  A Behavioral Homeostasis Theory of Habituation and Sensitization: II. Further Developments and Predictions , 2006, Reviews in the neurosciences.

[19]  Ben H. Jansen,et al.  Morphological and latency abnormalities of the mid-latency auditory evoked responses in schizophrenia: a preliminary report , 2004, Schizophrenia Research.

[20]  H. Hwu,et al.  More evidence to support the role of S2 in P50 studies , 2010, Schizophrenia Research.

[21]  Angela R. Laird,et al.  Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation , 2011, NeuroImage.

[22]  L. Petrinovich,et al.  Habituation, sensitization, and behavior , 1984 .

[23]  N. Boutros,et al.  Genetic and environmental influences on sensory gating of mid-latency auditory evoked responses: A twin study , 2007, Schizophrenia Research.

[24]  C. Elger,et al.  Sensory gating in epilepsy – Effects of the lateralization of hippocampal sclerosis , 2008, Clinical Neurophysiology.

[25]  B. Maher,et al.  Progress in experimental personality research , 1964 .

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

[27]  M. Davis,et al.  Comparison of response plasticity between the eyeblink and vertex potential in humans. , 1972, Electroencephalography and clinical neurophysiology.

[28]  M. Fuchs,et al.  Development of Volume Conductor and Source Models to Localize Epileptic Foci , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[29]  Kathy A. Low,et al.  Latent inhibition mediates N1 attenuation to repeating sounds. , 2004, Psychophysiology.

[30]  H. C. Cromwell,et al.  Auditory inhibitory gating in the amygdala: Single-unit analysis in the behaving rat , 2005, Brain Research.

[31]  Wen-Pin Chang,et al.  Probing the relative contribution of the first and second responses to sensory gating indices: a meta-analysis. , 2011, Psychophysiology.

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

[33]  C E Elger,et al.  Preoperative Evaluation for Epilepsy Surgery (Bonn Algorithm) , 2002, Zentralblatt fur Neurochirurgie.

[34]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

[35]  C. Shagass,et al.  CHAPTER 9 – Do Human Evoked Potentials Habituate? , 1984 .

[36]  T R Bashore,et al.  Attentional influence on the P50 component of the auditory event-related brain potential. , 1992, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[37]  Simon J Graham,et al.  Somatosensory Gating and Recovery From Stroke Involving the Thalamus , 2002, Stroke.

[38]  W. Atchley,et al.  Statistical Properties of Ratios. I. Empirical Results , 1976 .

[39]  Nash N. Boutros,et al.  P50 sensory gating ratios in schizophrenics and controls: A review and data analysis , 2008, Psychiatry Research.

[40]  J. Alpert,et al.  Neurophysiological studies of sensory gating in mania: comparison with schizophrenia. , 1983, Biological psychiatry.

[41]  S. Arnfred,et al.  Exploration of auditory P50 gating in schizophrenia by way of difference waves , 2006, Behavioral and Brain Functions.

[42]  A. Belger,et al.  Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating , 1999, Biological Psychiatry.

[43]  Thomas Grunwald,et al.  Neuronal substrates of sensory gating within the human brain , 2003, Biological Psychiatry.

[44]  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.

[45]  Timothy A. Pedley,et al.  Epilepsy : a comprehensive textbook , 2008 .

[46]  Timothy Edward John Behrens,et al.  Anatomical and Functional Connectivity of Cytoarchitectonic Areas within the Human Parietal Operculum , 2010, The Journal of Neuroscience.

[47]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[48]  N. Boutros,et al.  Supra-modal role for frontal cortex in sensory gating , 2007 .

[49]  N. Boutros,et al.  Range of sensory gating values and test-retest reliability in normal subjects. , 2007, Psychophysiology.

[50]  N. Boutros,et al.  Stimulus parameter effects on the P50 evoked response , 1992, Biological Psychiatry.

[51]  P. Trautner,et al.  Sensory gating in the human hippocampal and rhinal regions , 2005, Clinical Neurophysiology.

[52]  Scott Makeig,et al.  Neuroelectromagnetic Forward Head Modeling Toolbox , 2010, Journal of Neuroscience Methods.

[53]  H. C. Cromwell,et al.  Sensory Gating: A Translational Effort from Basic to Clinical Science , 2008, Clinical EEG and neuroscience.

[54]  Timm Rosburg,et al.  Mid-latency auditory-evoked responses and sensory gating in focal epilepsy: a preliminary exploration. , 2006, The Journal of neuropsychiatry and clinical neurosciences.

[55]  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.

[56]  Stephen H. D. Jackson.  INT CONGR SER , 2001 .

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

[58]  R Freedman,et al.  Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. , 1982, Biological psychiatry.

[59]  C. Im,et al.  Evaluation of Algorithms for Intracranial EEG (iEEG) Source Imaging of Extended Sources: Feasibility of Using iEEG Source Imaging for Localizing Epileptogenic Zones in Secondary Generalized Epilepsy , 2011, Brain Topography.

[60]  R. Freedman,et al.  Deficits in sensory gating in schizophrenic patients and their relatives. Evidence obtained with auditory evoked responses. , 1984, Archives of general psychiatry.

[61]  J. R. Hughes.  The Photoparoxysmal Response: The Probable Cause of Attacks during Video Games , 2008, Clinical EEG and neuroscience.

[62]  Nash N. Boutros,et al.  Relationships between sensory “gating out” and sensory “gating in” of auditory evoked potentials in schizophrenia: A pilot study , 2010, Schizophrenia Research.

[63]  R. Rothermel,et al.  Intracranial Recording and Source Localization of Auditory Brain Responses Elicited at the 50 ms Latency in Three Children Aged from 3 to 16 Years , 2009, Brain Topography.

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

[65]  M. Keshavan,et al.  Sensory-gating deficit of the N100 mid-latency auditory evoked potential in medicated schizophrenia patients , 2009, Schizophrenia Research.

[66]  Michael Krause,et al.  Auditory sensory gating in hippocampus and reticular thalamic neurons in anesthetized rats , 2003, Biological Psychiatry.

[67]  David A. Smith,et al.  Reliability of P50 auditory event-related potential indices of sensory gating. , 1994, Psychophysiology.

[68]  G. Fein,et al.  P50 suppression is not affected by attentional manipulations , 1992, Biological Psychiatry.

[69]  P. Venables,et al.  INPUT DYSFUNCTION IN SCHIZOPHRENIA. , 1964, Progress in experimental personality research.