Dynamic Oscillatory Processes Governing Cued Orienting and Allocation of Auditory Attention

In everyday listening situations, we need to constantly switch between alternative sound sources and engage attention according to cues that match our goals and expectations. The exact neuronal bases of these processes are poorly understood. We investigated oscillatory brain networks controlling auditory attention using cortically constrained fMRI-weighted magnetoencephalography/EEG source estimates. During consecutive trials, participants were instructed to shift attention based on a cue, presented in the ear where a target was likely to follow. To promote audiospatial attention effects, the targets were embedded in streams of dichotically presented standard tones. Occasionally, an unexpected novel sound occurred opposite to the cued ear to trigger involuntary orienting. According to our cortical power correlation analyses, increased frontoparietal/temporal 30–100 Hz gamma activity at 200–1400 msec after cued orienting predicted fast and accurate discrimination of subsequent targets. This sustained correlation effect, possibly reflecting voluntary engagement of attention after the initial cue-driven orienting, spread from the TPJ, anterior insula, and inferior frontal cortices to the right FEFs. Engagement of attention to one ear resulted in a significantly stronger increase of 7.5–15 Hz alpha in the ipsilateral than contralateral parieto-occipital cortices 200–600 msec after the cue onset, possibly reflecting cross-modal modulation of the dorsal visual pathway during audiospatial attention. Comparisons of cortical power patterns also revealed significant increases of sustained right medial frontal cortex theta power, right dorsolateral pFC and anterior insula/inferior frontal cortex beta power, and medial parietal cortex and posterior cingulate cortex gamma activity after cued versus novelty-triggered orienting (600–1400 msec). Our results reveal sustained oscillatory patterns associated with voluntary engagement of auditory spatial attention, with the frontoparietal and temporal gamma increases being best predictors of subsequent behavioral performance.

[1]  Marty G Woldorff,et al.  Timing and Sequence of Brain Activity in Top-Down Control of Visual-Spatial Attention , 2007, PLoS biology.

[2]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[3]  A. Burgess,et al.  Paradox lost? Exploring the role of alpha oscillations during externally vs. internally directed attention and the implications for idling and inhibition hypotheses. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  Iiro P. Jääskeläinen,et al.  Psychophysics and neuronal bases of sound localization in humans , 2014, Hearing Research.

[5]  Juha Salmi,et al.  Orienting and maintenance of spatial attention in audition and vision: an event‐related brain potential study , 2007, The European journal of neuroscience.

[6]  Markus Butz,et al.  Sustained gamma band synchronization in early visual areas reflects the level of selective attention , 2012, NeuroImage.

[7]  Claude Alain,et al.  Dissociable memory- and response-related activity in parietal cortex during auditory spatial working memory. , 2010, Frontiers in psychology.

[8]  J. Enns,et al.  Relations between covert orienting and filtering in the development of visual attention. , 1989, Journal of experimental child psychology.

[9]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[10]  Roger B. H. Tootell,et al.  The advantage of combining MEG and EEG: Comparison to fMRI in focally stimulated visual cortex , 2007, NeuroImage.

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

[12]  Nathan Weisz,et al.  Lateralized auditory cortical alpha band activity and interregional connectivity pattern reflect anticipation of target sounds. , 2012, Cerebral cortex.

[13]  James T. Townsend,et al.  Methods of Modeling Capacity in Simple Processing Systems , 2014 .

[14]  M. Posner,et al.  Components of visual orienting , 1984 .

[15]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  M. Cheal,et al.  Central and Peripheral Precuing of Forced-Choice Discrimination , 1991, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[17]  Nikita A. Novikov,et al.  Theta and Alpha Band Modulations Reflect Error-Related Adjustments in the Auditory Condensation Task , 2015, Front. Hum. Neurosci..

[18]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[20]  Jonas Obleser,et al.  Cortical alpha oscillations as a tool for auditory selective inhibition , 2014, Front. Hum. Neurosci..

[21]  Andreas K. Engel,et al.  Buildup of Choice-Predictive Activity in Human Motor Cortex during Perceptual Decision Making , 2009, Current Biology.

[22]  M. Woldorff,et al.  The neural circuitry underlying the executive control of auditory spatial attention , 2007, Brain Research.

[23]  S. Yantis,et al.  Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex. , 2007, Cerebral cortex.

[24]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[25]  A. Nobre,et al.  The dynamics of shifting visuospatial attention revealed by event-related potentials , 2000, Neuropsychologia.

[26]  S. Yantis,et al.  Cortical mechanisms of feature-based attentional control. , 2003, Cerebral cortex.

[27]  John J. Foxe,et al.  Oscillatory Sensory Selection Mechanisms during Intersensory Attention to Rhythmic Auditory and Visual Inputs: A Human Electrocorticographic Investigation , 2011, The Journal of Neuroscience.

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

[29]  H J Müller,et al.  Movement versus focusing of visual attention , 1989, Perception & psychophysics.

[30]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[31]  S. Hillyard,et al.  Electrical Signs of Selective Attention in the Human Brain , 1973, Science.

[32]  Karsten Specht,et al.  Attention and cognitive control networks assessed in a dichotic listening fMRI study , 2011, Brain and Cognition.

[33]  Dave R. M. Langers,et al.  Lateralization, connectivity and plasticity in the human central auditory system , 2005, NeuroImage.

[34]  V Solo,et al.  Dynamic Granger-Geweke causality modeling with application to interictal spike propagation , 2009, NeuroImage.

[35]  S. Hillyard,et al.  The effects of channel-selective attention on the mismatch negativity wave elicited by deviant tones. , 1991, Psychophysiology.

[36]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

[37]  Sarah Shomstein,et al.  Parietal Cortex Mediates Voluntary Control of Spatial and Nonspatial Auditory Attention , 2006, The Journal of Neuroscience.

[38]  Ole Jensen,et al.  Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli , 2011, Journal of Cognitive Neuroscience.

[39]  S. Wise,et al.  Motor aspects of cue-related neuronal activity in premotor cortex of the rhesus monkey , 1983, Brain Research.

[40]  Christian Büchel,et al.  Integration of local features to a global percept by neural coupling. , 2006, Cerebral cortex.

[41]  A Merisalo,et al.  Location vs. frequency of pure tones as a basis of fast discrimination. , 1980, Acta psychologica.

[42]  Teemu Rinne,et al.  Functional Maps of Human Auditory Cortex: Effects of Acoustic Features and Attention , 2009, PloS one.

[43]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

[44]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[45]  Jochen Kaiser,et al.  Effects of feature-selective attention on auditory pattern and location processing , 2008, NeuroImage.

[46]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[47]  R. Zatorre,et al.  Shifting and focusing auditory spatial attention. , 1995, Journal of experimental psychology. Human perception and performance.

[48]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[49]  E D Adrian,et al.  The interpretation of potential waves in the cortex , 1934, The Journal of physiology.

[50]  Hannu Tiitinen,et al.  Suppression of transient 40-Hz auditory response by haloperidol suggests modulation of human selective attention by dopamine D2 receptors , 2000, Neuroscience Letters.

[51]  Simone Cardoso Synchronization of Neuronal Activity during Stimulus Expectation in a Direction Discrimination Task , 1997 .

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

[53]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[54]  Eric Maris,et al.  Attentional Cues Affect Accuracy and Reaction Time via Different Cognitive and Neural Processes , 2012, The Journal of Neuroscience.

[55]  Lucas Spierer,et al.  Hemispheric competence for auditory spatial representation. , 2009, Brain : a journal of neurology.

[56]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[57]  I. THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[58]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

[59]  Matthew F. S. Rushworth,et al.  Components of Switching Intentional Set , 2002, Journal of Cognitive Neuroscience.

[60]  Chris Rorden,et al.  Spatial Attention Evokes Similar Activation Patterns for Visual and Auditory Stimuli , 2010, Journal of Cognitive Neuroscience.

[61]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[62]  Iiro P. Jääskeläinen,et al.  Dissociable Influences of Auditory Object vs. Spatial Attention on Visual System Oscillatory Activity , 2012, PloS one.

[63]  Yan Zhang,et al.  Prestimulus Cortical Activity is Correlated with Speed of Visuomotor Processing , 2008, Journal of Cognitive Neuroscience.

[64]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[65]  D Deutsch,et al.  Binaural integration of melodic patterns , 1979, Perception & psychophysics.

[66]  M. Posner,et al.  Research on attention networks as a model for the integration of psychological science. , 2007, Annual review of psychology.

[67]  G. R Mangun,et al.  Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping , 2000, Clinical Neurophysiology.

[68]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[69]  C. Gerloff,et al.  Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range , 2007, The European journal of neuroscience.

[70]  Philippe Kahane,et al.  Efficient “Pop-Out” Visual Search Elicits Sustained Broadband Gamma Activity in the Dorsal Attention Network , 2012, The Journal of Neuroscience.

[71]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[72]  J. Fritz,et al.  Active listening: Task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex , 2005, Hearing Research.

[73]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[74]  Teemu Rinne,et al.  Task-Dependent Activations of Human Auditory Cortex during Pitch Discrimination and Pitch Memory Tasks , 2009, The Journal of Neuroscience.

[75]  Lucas Spierer,et al.  The role of the right parietal cortex in sound localization: A chronometric single pulse transcranial magnetic stimulation study , 2011, Neuropsychologia.

[76]  A S Bregman,et al.  Auditory streaming is cumulative. , 1978, Journal of experimental psychology. Human perception and performance.

[77]  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.

[78]  R. Knight Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

[79]  E. Schröger,et al.  Attentional orienting and reorienting is indicated by human event‐related brain potentials , 1998, Neuroreport.

[80]  Jan Theeuwes,et al.  Endogenous and exogenous attention shifts are mediated by the same large-scale neural network , 2004, NeuroImage.

[81]  Risto Näätänen,et al.  Hemispheric lateralization of cerebral blood-flow changes during selective listening to dichotically presented continuous speech. , 2003, Brain research. Cognitive brain research.

[82]  Aniruddh D. Patel,et al.  Top‐Down Control of Rhythm Perception Modulates Early Auditory Responses , 2009, Annals of the New York Academy of Sciences.

[83]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

[84]  G Pfurtscheller,et al.  Induced Oscillations in the Alpha Band: Functional Meaning , 2003, Epilepsia.

[85]  O. Salonen,et al.  Brain networks of bottom-up triggered and top-down controlled shifting of auditory attention , 2009, Brain Research.

[86]  J. Bouyer,et al.  [Relationship between attention and mu rhythms in the cat and the monkey (author's transl)]. , 1979, Revue d'electroencephalographie et de neurophysiologie clinique.

[87]  Werner Lutzenberger,et al.  Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli , 2006, NeuroImage.

[88]  S. Bentin,et al.  Different Effects of Voluntary and Involuntary Attention on EEG Activity in the Gamma Band , 2007, The Journal of Neuroscience.

[89]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[90]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[91]  R Näätänen,et al.  Replicability of MEG and EEG measures of the auditory N1/N1m-response. , 1998, Electroencephalography and clinical neurophysiology.

[92]  Cheryl L. Grady,et al.  The contribution of the inferior parietal lobe to auditory spatial working memory , 2008 .

[93]  Josef Ling,et al.  Evoked and intrinsic asymmetries during auditory attention: implications for the contralateral and neglect models of functioning. , 2013, Cerebral cortex.

[94]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[95]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[96]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[97]  E. Halgren,et al.  Cancellation of EEG and MEG signals generated by extended and distributed sources , 2009, Human brain mapping.

[98]  M. Montaron,et al.  Relations entre l'attention et le rythme mu chez le chat et le singe* , 1979 .

[99]  Gregor Leicht,et al.  Auditory cortex and anterior cingulate cortex sources of the early evoked gamma-band response: Relationship to task difficulty and mental effort , 2007, Neuropsychologia.

[100]  Matti S. Hämäläinen,et al.  Lateralized parietotemporal oscillatory phase synchronization during auditory selective attention , 2014, NeuroImage.

[101]  O. Bertrand,et al.  Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. , 2005, Cerebral cortex.

[102]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[103]  C. Spence,et al.  Tactile-Visual Links in Exogenous Spatial Attention under Different Postures: Convergent Evidence from Psychophysics and ERPs , 2001, Journal of Cognitive Neuroscience.

[104]  C Alain,et al.  Location and frequency cues in auditory selective attention. , 2001, Journal of experimental psychology. Human perception and performance.

[105]  H Shibasaki,et al.  Role of the primary auditory cortex in auditory selective attention studied by whole-head neuromagnetometer. , 1998, Brain research. Cognitive brain research.

[106]  D. Bouwhuis,et al.  Attention and performance X : control of language processes , 1986 .

[107]  Eric Larson,et al.  The cortical dynamics underlying effective switching of auditory spatial attention , 2013, NeuroImage.

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

[109]  John J. Foxe,et al.  Attention-dependent suppression of distracter visual input can be cross-modally cued as indexed by anticipatory parieto-occipital alpha-band oscillations. , 2001, Brain research. Cognitive brain research.

[110]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[111]  John J. Foxe,et al.  Oscillatory Alpha-Band Mechanisms and the Deployment of Spatial Attention to Anticipated Auditory and Visual Target Locations: Supramodal or Sensory-Specific Control Mechanisms? , 2011, The Journal of Neuroscience.

[112]  Bruce D. McCandliss,et al.  The Relation of Brain Oscillations to Attentional Networks , 2007, The Journal of Neuroscience.

[113]  Daphne N. Yu,et al.  High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. , 1997, Cerebral cortex.

[114]  Jyrki Ahveninen,et al.  Brain Networks of Novelty-Driven Involuntary and Cued Voluntary Auditory Attention Shifting , 2012, PloS one.

[115]  R. Klein,et al.  Inhibition of return , 2000, Trends in Cognitive Sciences.

[116]  Werner Lutzenberger,et al.  Dynamics of gamma-band activity in human magnetoencephalogram during auditory pattern working memory , 2003, NeuroImage.

[117]  Mikko Sams,et al.  Attention-driven auditory cortex short-term plasticity helps segregate relevant sounds from noise , 2011, Proceedings of the National Academy of Sciences.

[118]  M. D'Zmura,et al.  Lateralization of Frequency-Specific Networks for Covert Spatial Attention to Auditory Stimuli , 2011, Brain Topography.

[119]  A. Dale,et al.  Distributed current estimates using cortical orientation constraints , 2006, Human brain mapping.

[120]  L. M. Ward,et al.  Theta modulation of inter-regional gamma synchronization during auditory attention control , 2012, Brain Research.

[121]  C. Darwin Auditory grouping , 1997, Trends in Cognitive Sciences.

[122]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[123]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[124]  S. Keele,et al.  Changing internal constraints on action: the role of backward inhibition. , 2000, Journal of experimental psychology. General.

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

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

[127]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[128]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[129]  A. Brzezicka,et al.  β band oscillations engagement in human alertness process. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[130]  Michael X. Cohen,et al.  Fronto-parietal network oscillations reveal relationship between working memory capacity and cognitive control , 2014, Front. Hum. Neurosci..

[131]  Shlomit Yuval-Greenberg,et al.  Scalp-Recorded Induced Gamma-Band Responses to Auditory Stimulation and Its Correlations with Saccadic Muscle-Activity , 2011, Brain Topography.

[132]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[133]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[134]  Alan C. Evans,et al.  Auditory Attention to Space and Frequency Activates Similar Cerebral Systems , 1999, NeuroImage.

[135]  John C. Adair,et al.  The neural networks underlying endogenous auditory covert orienting and reorienting , 2006, NeuroImage.

[136]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[137]  Matthew G. Wisniewski,et al.  Brain dynamics that correlate with effects of learning on auditory distance perception , 2014, Front. Neurosci..