Acoustic and higher-level representations of naturalistic auditory scenes in human auditory and frontal cortex

&NA; Often, in everyday life, we encounter auditory scenes comprising multiple simultaneous sounds and succeed to selectively attend to only one sound, typically the most relevant for ongoing behavior. Studies using basic sounds and two‐talker stimuli have shown that auditory selective attention aids this by enhancing the neural representations of the attended sound in auditory cortex. It remains unknown, however, whether and how this selective attention mechanism operates on representations of auditory scenes containing natural sounds of different categories. In this high‐field fMRI study we presented participants with simultaneous voices and musical instruments while manipulating their focus of attention. We found an attentional enhancement of neural sound representations in temporal cortex ‐ as defined by spatial activation patterns ‐ at locations that depended on the attended category (i.e., voices or instruments). In contrast, we found that in frontal cortex the site of enhancement was independent of the attended category and the same regions could flexibly represent any attended sound regardless of its category. These results are relevant to elucidate the interacting mechanisms of bottom‐up and top‐down processing when listening to real‐life scenes comprised of multiple sound categories. HighlightsInvestigated selective attention to sounds of various categories in auditory scenes.Measured the associated cortical activity with high‐field fMRI.Quantified category selective pattern enhancement in auditory and frontal cortex.Location of enhancement in temporal cortex depends on the attended category.Same regions in frontal cortex are enhanced independent of the attended category.

[1]  John J. Foxe,et al.  Attentional Selection in a Cocktail Party Environment Can Be Decoded from Single-Trial EEG. , 2015, Cerebral cortex.

[2]  J. Simon,et al.  Emergence of neural encoding of auditory objects while listening to competing speakers , 2012, Proceedings of the National Academy of Sciences.

[3]  Li Fei-Fei,et al.  Neural mechanisms of rapid natural scene categorization in human visual cortex , 2009, Nature.

[4]  Paul Boersma,et al.  Praat: doing phonetics by computer , 2003 .

[5]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[6]  Jeffrey S. Johnson,et al.  Active Engagement Improves Primary Auditory Cortical Neurons' Ability to Discriminate Temporal Modulation , 2012, The Journal of Neuroscience.

[7]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[8]  Christopher W. Bishop,et al.  Pattern of BOLD signal in auditory cortex relates acoustic response to perceptual streaming , 2011, BMC Neuroscience.

[9]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[10]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[12]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  S. David,et al.  Auditory attention : focusing the searchlight on sound , 2007 .

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

[16]  Gregory Hickok,et al.  Redefining the Functional Organization of the Planum Temporale Region: Space, Objects, and Sensory–Motor Integration , 2012 .

[17]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[18]  T. Griffiths,et al.  The planum temporale as a computational hub , 2002, Trends in Neurosciences.

[19]  Albert S. Bregman,et al.  The Auditory Scene. (Book Reviews: Auditory Scene Analysis. The Perceptual Organization of Sound.) , 1990 .

[20]  Y. Cohen,et al.  Neural mechanisms of auditory categorization: from across brain areas to within local microcircuits , 2014, Front. Neurosci..

[21]  T. Griffiths,et al.  What is an auditory object? , 2004, Nature Reviews Neuroscience.

[22]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[23]  Rhodri Cusack,et al.  The Intraparietal Sulcus and Perceptual Organization , 2005, Journal of Cognitive Neuroscience.

[24]  J. Rauschecker,et al.  Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category , 2010, The Journal of Neuroscience.

[25]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[26]  Pascal Belin,et al.  Learning-induced changes in the cerebral processing of voice identity. , 2011, Cerebral cortex.

[27]  S. David,et al.  Rapid Synaptic Depression Explains Nonlinear Modulation of Spectro-Temporal Tuning in Primary Auditory Cortex by Natural Stimuli , 2009, The Journal of Neuroscience.

[28]  Claude Alain,et al.  Assessing the auditory dual-pathway model in humans , 2004, NeuroImage.

[29]  Paul Boersma,et al.  Praat, a system for doing phonetics by computer , 2002 .

[30]  E. Formisano,et al.  Frequency‐Selective Attention in Auditory Scenes Recruits Frequency Representations Throughout Human Superior Temporal Cortex , 2016, Cerebral cortex.

[31]  Y. Benjamini,et al.  Screening for Partial Conjunction Hypotheses , 2008, Biometrics.

[32]  R. Goebel,et al.  Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex , 2013, The Journal of Neuroscience.

[33]  Lee M. Miller,et al.  A Multisensory Cortical Network for Understanding Speech in Noise , 2009, Journal of Cognitive Neuroscience.

[34]  R. Zatorre,et al.  Where is 'where' in the human auditory cortex? , 2002, Nature Neuroscience.

[35]  David J. Freedman,et al.  Dynamic population coding of category information in inferior temporal and prefrontal cortex. , 2008, Journal of neurophysiology.

[36]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[37]  R. Desimone,et al.  A backward progression of attentional effects in the ventral stream , 2009, Proceedings of the National Academy of Sciences.

[38]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[39]  N. Mesgarani,et al.  Selective cortical representation of attended speaker in multi-talker speech perception , 2012, Nature.

[40]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[41]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[42]  Lee M. Miller,et al.  Auditory attentional control and selection during cocktail party listening. , 2010, Cerebral cortex.

[43]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[44]  S. Kastner,et al.  A neural basis for real-world visual search in human occipitotemporal cortex , 2011, Proceedings of the National Academy of Sciences.

[45]  S. Hochstein,et al.  Reverse hierarchies and sensory learning , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[47]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[48]  Tobias Kober,et al.  MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field , 2010, NeuroImage.

[49]  Jefferson E. Roy,et al.  Representation of Multiple, Independent Categories in the Primate Prefrontal Cortex , 2010, Neuron.

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

[51]  Noël Staeren,et al.  Sound Categories Are Represented as Distributed Patterns in the Human Auditory Cortex , 2009, Current Biology.

[52]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[53]  Yinjuan Du,et al.  Noise differentially impacts phoneme representations in the auditory and speech motor systems , 2014, Proceedings of the National Academy of Sciences.

[54]  C. Schroeder,et al.  The Spectrotemporal Filter Mechanism of Auditory Selective Attention , 2013, Neuron.

[55]  Daniel S. O'Leary,et al.  An MRI-Based Parcellation Method for the Temporal Lobe , 2000, NeuroImage.

[56]  Y. Cohen,et al.  The what, where and how of auditory-object perception , 2013, Nature Reviews Neuroscience.

[57]  B. Shinn-Cunningham Object-based auditory and visual attention , 2008, Trends in Cognitive Sciences.

[58]  M. Schönwiesner,et al.  Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI , 2009, Proceedings of the National Academy of Sciences.

[59]  R. Carlyon,et al.  Effects of location, frequency region, and time course of selective attention on auditory scene analysis. , 2004, Journal of experimental psychology. Human perception and performance.

[60]  S. Shamma,et al.  Temporal coherence and attention in auditory scene analysis , 2011, Trends in Neurosciences.

[61]  Christian J. Sumner,et al.  Examining the role of frequency specificity in the enhancement and suppression of human cortical activity by auditory selective attention , 2009, Hearing Research.

[62]  D. Poeppel,et al.  Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party” , 2013, Neuron.

[63]  S. David,et al.  Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex , 2014, Neuron.

[64]  Teemu Rinne,et al.  Stimulus-dependent activations and attention-related modulations in the auditory cortex: A meta-analysis of fMRI studies , 2014, Hearing Research.

[65]  Brian E. Russ,et al.  A functional role for the ventrolateral prefrontal cortex in non-spatial auditory cognition , 2009, Proceedings of the National Academy of Sciences.

[66]  T. Hackett Information flow in the auditory cortical network , 2011, Hearing Research.

[67]  Lee M. Miller,et al.  Tuning In to Sound: Frequency-Selective Attentional Filter in Human Primary Auditory Cortex , 2013, The Journal of Neuroscience.

[68]  Ramesh Srinivasan,et al.  Suppression of competing speech through entrainment of cortical oscillations. , 2013, Journal of neurophysiology.

[69]  David Poeppel,et al.  The cortical analysis of speech-specific temporal structure revealed by responses to sound quilts , 2015, Nature Neuroscience.

[70]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[71]  Gregory Hickok,et al.  Auditory Spatial and Object Processing in the Human Planum Temporale: No Evidence for Selectivity , 2010, Journal of Cognitive Neuroscience.

[72]  J. Simon,et al.  Neural coding of continuous speech in auditory cortex during monaural and dichotic listening. , 2012, Journal of neurophysiology.

[73]  Gregory B. Cogan,et al.  Visual Input Enhances Selective Speech Envelope Tracking in Auditory Cortex at a “Cocktail Party” , 2013, The Journal of Neuroscience.

[74]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[75]  Bruno L. Giordano,et al.  Automatic domain-general processing of sound source identity in the left posterior middle frontal gyrus , 2014, Cortex.

[76]  Josh H. McDermott,et al.  Distinct Cortical Pathways for Music and Speech Revealed by Hypothesis-Free Voxel Decomposition , 2015, Neuron.

[77]  M. Chait,et al.  Brain Bases for Auditory Stimulus-Driven Figure–Ground Segregation , 2011, The Journal of Neuroscience.

[78]  Antoine J. Shahin,et al.  Attentional Gain Control of Ongoing Cortical Speech Representations in a “Cocktail Party” , 2010, The Journal of Neuroscience.

[79]  Arafat Angulo-Perkins,et al.  Music listening engages specific cortical regions within the temporal lobes: Differences between musicians and non-musicians , 2014, Cortex.