Spatiotemporal properties of auditory intensity processing in multisensor MEG

Loudness dependence of auditory evoked potentials (LDAEP) evaluates loudness processing in the human auditory system and is often altered in patients with psychiatric disorders. Previous research has suggested that this measure may be used as an indicator of the central serotonergic system through the highly serotonergic innervation of the auditory cortex. However, differences among the commonly used analysis approaches (such as source analysis and single electrode estimation) may lead to different results. Putatively due to discrepancies of the underlying structures being measured. Therefore, it is important to learn more about how and where in the brain loudness variation is processed. We conducted a detailed investigation of the LDAEP generators and their temporal dynamics by means of multichannel magnetoencephalography (MEG). Evoked responses to brief tones of five different intensities were recorded from 19 healthy participants. We used magnetic field tomography in order to appropriately localize superficial as well as deep source generators of which we conducted a time series analysis. The results showed that apart from the auditory cortex other cortical sources exhibited activation during the N1/P2 time window. Analysis of time courses in the regions of interest revealed a sequential cortical activation from primary sensory areas, particularly the auditory and somatosensory cortex to posterior cingulate cortex (PCC) and to premotor cortex (PMC). The additional activation within the PCC and PMC has implications on the analysis approaches used in LDAEP research.

[1]  Young-Min Park,et al.  The loudness dependence of the auditory evoked potential (LDAEP) in schizophrenia, bipolar disorder, major depressive disorder, anxiety disorder, and healthy controls , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[2]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[3]  B. Müller,et al.  The intensity dependence of the auditory evoked N1 component as a predictor of reponse to Citalopram treatment in patients with major depression , 2004, Neuroscience Letters.

[4]  M. Buchsbaum,et al.  The effects of attention, stimulus intensity, and individual differences on the average evoked response. , 1973, Psychophysiology.

[5]  Eun Jin Park The Loudness Dependence of the Auditory Evoked Potential in Children with ADHD , 2013 .

[6]  Georg Juckel,et al.  Intensity dependence of auditory evoked potentials as an indicator of central serotonergic neurotransmission: A new hypothesis , 1993, Biological Psychiatry.

[7]  G. V. Van Hoesen,et al.  Neural connections of the posteromedial cortex in the macaque , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[8]  U Hegerl,et al.  Comparison between the analysis of the loudness dependency of the auditory N1/P2 component with LORETA and dipole source analysis in the prediction of treatment response to the selective serotonin reuptake inhibitor citalopram in major depression , 2002, Clinical Neurophysiology.

[9]  M Reite,et al.  Auditory evoked magnetic fields: response amplitude vs. stimulus intensity. , 1982, Electroencephalography and clinical neurophysiology.

[10]  J Leon Kenemans,et al.  How Human Electrophysiology Informs Psychopharmacology: from Bottom-up Driven Processing to Top-Down Control , 2011, Neuropsychopharmacology.

[11]  Karl J. Friston,et al.  Variational Bayesian inversion of the equivalent current dipole model in EEG/MEG , 2008, NeuroImage.

[12]  Stefan Uppenkamp,et al.  Human auditory neuroimaging of intensity and loudness , 2014, Hearing Research.

[13]  Christoph Mulert,et al.  Association of catechol‐O‐methyltransferase variants with loudness dependence of auditory evoked potentials , 2008, Human psychopharmacology.

[14]  Steven W. Smith,et al.  The Scientist and Engineer's Guide to Digital Signal Processing , 1997 .

[15]  A. Simmons,et al.  Escitalopram attenuates posterior cingulate activity during self-evaluation in healthy volunteers , 2010, Psychiatry Research: Neuroimaging.

[16]  Daniel Senkowski,et al.  Allelic Variants of the Functional Promoter Polymorphism of the Human Serotonin Transporter Gene is Associated with Auditory Cortical Stimulus Processing , 2003, Neuropsychopharmacology.

[17]  M. Scherg,et al.  Two bilateral sources of the late AEP as identified by a spatio-temporal dipole model. , 1985, Electroencephalography and clinical neurophysiology.

[18]  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.

[19]  A. Schleicher,et al.  Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry , 2002, European Neuropsychopharmacology.

[20]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[21]  Natalia Jaworska,et al.  Response prediction to antidepressants using scalp and source-localized loudness dependence of auditory evoked potential (LDAEP) slopes , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[22]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[23]  S. Nakagawa,et al.  Auditory evoked responses in human auditory cortex to the variation of sound intensity in an ongoing tone , 2012, Hearing Research.

[24]  Andreas A. Ioannides,et al.  Real-time neural activity and connectivity in healthy individuals and schizophrenia patients , 2004, NeuroImage.

[25]  S. Posse,et al.  Intensity coding of auditory stimuli: an fMRI study , 1998, Neuropsychologia.

[26]  G. Kranz,et al.  Differential modulation of the default mode network via serotonin-1A receptors , 2012, Proceedings of the National Academy of Sciences.

[27]  Andreas A Ioannides,et al.  Magnetoencephalography as a Research Tool in Neuroscience: State of the Art , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[28]  V. Pascalis,et al.  Effects of personality trait emotionality on acoustic startle response and prepulse inhibition including N100 and P200 event-related potential , 2013, Clinical Neurophysiology.

[29]  John J. Foxe,et al.  Multisensory contributions to low-level, ‘unisensory’ processing , 2005, Current Opinion in Neurobiology.

[30]  Pia Baldinger,et al.  Gray matter and intrinsic network changes in the posterior cingulate cortex after selective serotonin reuptake inhibitor intake , 2014, NeuroImage.

[31]  R. Burkard,et al.  The functional anatomy of the normal human auditory system: responses to 0.5 and 4.0 kHz tones at varied intensities. , 1999, Cerebral cortex.

[32]  A. Ioannides,et al.  Continuous probabilistic solutions to the biomagnetic inverse problem , 1990 .

[33]  D. Sharp,et al.  The role of the posterior cingulate cortex in cognition and disease. , 2014, Brain : a journal of neurology.

[34]  J. Laurent,et al.  The effect of selective attention on augmenting/intensity function of the early negative waves of AEPs. , 1987, Electroencephalography and clinical neurophysiology. Supplement.

[35]  Young-Min Park,et al.  The loudness dependence of the auditory evoked potential (LDAEP) as a predictor of the response to escitalopram in patients with generalized anxiety disorder , 2011, Psychopharmacology.

[36]  Christoph Mulert,et al.  Sound level dependence of the primary auditory cortex: Simultaneous measurement with 61-channel EEG and fMRI , 2005, NeuroImage.

[37]  M. Bradley,et al.  Emotion, attention, and the startle reflex. , 1990, Psychological review.

[38]  Georg Juckel,et al.  [Insights in the central serotonergic function in patients with affective disorders]. , 2008, Neuropsychiatrie : Klinik, Diagnostik, Therapie und Rehabilitation : Organ der Gesellschaft Osterreichischer Nervenarzte und Psychiater.

[39]  F. Perrin,et al.  Dissociation of temporal and frontal components in the human auditory N1 wave: a scalp current density and dipole model analysis. , 1994, Electroencephalography and clinical neurophysiology.

[40]  P. Heil,et al.  Stimulation-history effects on the M100 revealed by its differential dependence on the stimulus onset interval. , 2012, Psychophysiology.

[41]  M Velasco,et al.  Subcortical correlates of the somatic, auditory and visual vertex activities. II. Referential EEG responses. , 1986, Electroencephalography and clinical neurophysiology.

[42]  H. Neville,et al.  Auditory and visual refractory period effects in children and adults: An ERP study , 2005, Clinical Neurophysiology.

[43]  Christoph Mulert,et al.  Differential prediction of first clinical response to serotonergic and noradrenergic antidepressants using the loudness dependence of auditory evoked potentials in patients with major depressive disorder. , 2007, The Journal of clinical psychiatry.

[44]  D. Woods The component structure of the N1 wave of the human auditory evoked potential. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[45]  John G. Neuhoff,et al.  Spatiotemporal Pattern of Neural Processing in the Human Auditory Cortex , 2002, Science.

[46]  M J Campbell,et al.  The monoaminergic innervation of primate neocortex. , 1986, Human neurobiology.

[47]  R. Croft,et al.  The loudness dependence of the auditory evoked potential (LDAEP) as an in vivo biomarker of central serotonergic function in humans: rationale, evaluation and review of findings , 2008, Human psychopharmacology.

[48]  Peter A. Tass,et al.  A new toolbox for combining magnetoencephalographic source analysis and cytoarchitectonic probabilistic data for anatomical classification of dynamic brain activity , 2007, NeuroImage.

[49]  G. R. Fink,et al.  The temporal dynamics of the Müller-Lyer illusion. , 2010, Cerebral cortex.

[50]  M. Scherg,et al.  Intracerebral Sources of Human Auditory-Evoked Potentials , 1999, Audiology and Neurotology.

[51]  John G. Taylor,et al.  Mathematical analysis of lead field expansions , 1999, IEEE Transactions on Medical Imaging.

[52]  P. Berg,et al.  Use of prior knowledge in brain electromagnetic source analysis , 2005, Brain Topography.

[53]  J. Ahveninen,et al.  Acute trytophan depletion decreases intensity dependence of auditory evoked magnetic N1/P2 dipole source activity , 2002, Psychopharmacology.

[54]  H. Vaughan,et al.  The sources and intracerebral distribution of auditory evoked potentials in the alert rhesus monkey , 1975, Brain Research.

[55]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[56]  Irina S. Sigalovsky,et al.  Effects of sound level on fMRI activation in human brainstem, thalamic and cortical centers , 2006, Hearing Research.

[57]  E. Azmitia,et al.  The primate serotonergic system: a review of human and animal studies and a report on Macaca fascicularis. , 1986, Advances in neurology.

[58]  S. Hillyard,et al.  The effects of frontal and temporal-parietal lesions on the auditory evoked potential in man. , 1980, Electroencephalography and clinical neurophysiology.

[59]  S. Nakagawa,et al.  Sound level-dependent growth of N1m amplitude with low and high-frequency tones , 2009, Neuroreport.

[60]  André Brechmann,et al.  Sound-level-dependent representation of frequency modulations in human auditory cortex: a low-noise fMRI study. , 2002, Journal of neurophysiology.

[61]  M. Hallett,et al.  The relative metabolic demand of inhibition and excitation , 2000, Nature.

[62]  Timothy P. L. Roberts,et al.  The temporal dynamics of insula activity to disgust and happy facial expressions: A magnetoencephalography study , 2009, NeuroImage.

[63]  Felix Darvas,et al.  Determination of the loudness dependence of auditory evoked potentials: single‐electrode estimation versus dipole source analysis , 2011, Human psychopharmacology.

[64]  D Mrowinski,et al.  Intensity dependence of auditory evoked dipole source activity. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[65]  A R Palmer,et al.  Functional magnetic resonance imaging measurements of sound-level encoding in the absence of background scanner noise. , 2001, The Journal of the Acoustical Society of America.

[66]  A. Ioannides,et al.  Neuromagnetic Localization of CMV Generators Using Incomplete and Full-Head Biomagnetometer , 2000, NeuroImage.

[67]  John Öhrvik,et al.  Role of Monoamine Oxidase A Genotype and Psychosocial Factors in Male Adolescent Criminal Activity , 2006, Biological Psychiatry.

[68]  Guangying K. Wu,et al.  From elementary synaptic circuits to information processing in primary auditory cortex , 2011, Neuroscience & Biobehavioral Reviews.

[69]  Georg Juckel,et al.  The loudness dependence of auditory evoked potentials and effects of psychopathology and psychopharmacotherapy in psychiatric inpatients , 2012, Human psychopharmacology.

[70]  Siegfried Kasper,et al.  Lateralization of the serotonin-1A receptor distribution in language areas revealed by PET , 2009, NeuroImage.

[71]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[72]  Hisayuki Ojima,et al.  Interplay of excitation and inhibition elicited by tonal stimulation in pyramidal neurons of primary auditory cortex , 2011, Neuroscience & Biobehavioral Reviews.

[73]  D. Hall,et al.  Heschl’s gyrus is more sensitive to tone level than non-primary auditory cortex , 2002, Hearing Research.

[74]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[75]  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.

[76]  Frank Boers,et al.  Cortical Response Variation with Different Sound Pressure Levels: A Combined Event-Related Potentials and fMRI Study , 2014, PloS one.

[77]  C. Elberling,et al.  Auditory magnetic fields from the human cerebral cortex: Location and strength of an equivalent current dipole , 1982, Acta neurologica Scandinavica.

[78]  Baribeau Jc,et al.  The effect of selective attention on augmenting/intensity function of the early negative waves of AEPs. , 1987 .

[79]  B. Jacobs,et al.  Structure and function of the brain serotonin system. , 1992, Physiological reviews.

[80]  M. Buchsbaum,et al.  Individual differences in stimulus intensity response. , 1971, Psychophysiology.

[81]  S. Roux,et al.  Frontal auditory evoked potentials and augmenting-reducing. , 1985, Electroencephalography and clinical neurophysiology.

[82]  T W Picton,et al.  Separation and identification of event-related potential components by brain electric source analysis. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[83]  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.

[84]  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.

[85]  André Beauducel,et al.  Is auditory evoked potential augmenting/reducing affected by acute tryptophan depletion? , 2002, Biological Psychology.

[86]  G. Karmos,et al.  Auditory-evoked potentials as indicator of brain serotonergic activity first evidence in behaving cats , 1997, Biological Psychiatry.

[87]  Dave R. M. Langers,et al.  fMRI activation in relation to sound intensity and loudness , 2007, NeuroImage.

[88]  A. Friederici,et al.  Head models and dynamic causal modeling of subcortical activity using magnetoencephalographic/electroencephalographic data , 2012, Reviews in the neurosciences.

[89]  Simon B Eickhoff,et al.  Electrophysiology meets fMRI: Neural correlates of the startle reflex assessed by simultaneous EMG–fMRI data acquisition , 2010, Human brain mapping.

[90]  W. Herrmann,et al.  Comparison of the Amplitude/Intensity Function of the Auditory Evoked N1m and N1 Components , 2002, Neuropsychobiology.

[91]  L. C. Liu,et al.  Magnetic field tomography of cortical and deep processes: examples of "real-time mapping" of averaged and single trial MEG signals. , 1995, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[92]  Andreas Heinz,et al.  Loudness Dependence of Auditory Evoked Potentials as Indicator of Central Serotonergic Neurotransmission: Simultaneous Electrophysiological Recordings and In Vivo Microdialysis in the Rat Primary Auditory Cortex , 2008, Neuropsychopharmacology.

[93]  W. Kawohl,et al.  Examination of the effect of acute levodopa administration on the loudness dependence of auditory evoked potentials (LDAEP) in humans , 2011, Psychopharmacology.

[94]  P. Chauvel,et al.  Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients , 2001, Clinical Neurophysiology.

[95]  Erich Seifritz,et al.  The Loudness Dependence of Auditory Evoked Potentials (LDAEP) as an Indicator of Serotonergic Dysfunction in Patients with Predominant Schizophrenic Negative Symptoms , 2013, PloS one.

[96]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[97]  J. Pernier,et al.  Two separate frontal components in the N1 wave of the human auditory evoked response. , 1994, Psychophysiology.

[98]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[99]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[100]  M S Hämäläinen,et al.  Effects of intensity variation on human auditory evoked magnetic fields. , 1995, Acta oto-laryngologica.

[101]  Bernhard W. Müller,et al.  The intensity dependence of the auditory evoked N1/P2-ERP-component increases in pharmacotherapy of major depression with citalopram , 2004 .