DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Invariance to background noise as a signature of non-primary auditory cortex

Abstract

Despite well-established anatomical differences between primary and non-primary auditory cortex, the associated representational transformations have remained elusive. Here we show that primary and non-primary auditory cortex are differentiated by their invariance to real-world background noise. We measured fMRI responses to natural sounds presented in isolation and in real-world noise, quantifying invariance as the correlation between the two responses for individual voxels. Non-primary areas were substantially more noise-invariant than primary areas. This primary-nonprimary difference occurred both for speech and non-speech sounds and was unaffected by a concurrent demanding visual task, suggesting that the observed invariance is not specific to speech processing and is robust to inattention. The difference was most pronounced for real-world background noise—both primary and non-primary areas were relatively robust to simple types of synthetic noise. Our results suggest a general representational transformation between auditory cortical stages, illustrating a representational consequence of hierarchical organization in the auditory system.

Authors:
 [1]; ORCiD logo [2]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). McGovern Inst. for Brain Research, Center for Brains, Minds, and Machines; Columbia Univ., New York, NY (United States). Zuckerman Inst. of Mind, Brain, and Behavior
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). McGovern Inst. for Brain Research, Center for Brains, Minds, and Machines; Harvard Univ., Boston, MA (United States)
Publication Date:
Research Org.:
Krell Institute, Ames, IA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1610345
Grant/Contract Number:  
FG02-97ER25308; 1R01DC014739-01A1; R25GM067110; BCS-1634050; PHY17-48958
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Kell, Alexander J. E., and McDermott, Josh H. Invariance to background noise as a signature of non-primary auditory cortex. United States: N. p., 2019. Web. doi:10.1038/s41467-019-11710-y.
Kell, Alexander J. E., & McDermott, Josh H. Invariance to background noise as a signature of non-primary auditory cortex. United States. https://doi.org/10.1038/s41467-019-11710-y
Kell, Alexander J. E., and McDermott, Josh H. Mon . "Invariance to background noise as a signature of non-primary auditory cortex". United States. https://doi.org/10.1038/s41467-019-11710-y. https://www.osti.gov/servlets/purl/1610345.
@article{osti_1610345,
title = {Invariance to background noise as a signature of non-primary auditory cortex},
author = {Kell, Alexander J. E. and McDermott, Josh H.},
abstractNote = {Despite well-established anatomical differences between primary and non-primary auditory cortex, the associated representational transformations have remained elusive. Here we show that primary and non-primary auditory cortex are differentiated by their invariance to real-world background noise. We measured fMRI responses to natural sounds presented in isolation and in real-world noise, quantifying invariance as the correlation between the two responses for individual voxels. Non-primary areas were substantially more noise-invariant than primary areas. This primary-nonprimary difference occurred both for speech and non-speech sounds and was unaffected by a concurrent demanding visual task, suggesting that the observed invariance is not specific to speech processing and is robust to inattention. The difference was most pronounced for real-world background noise—both primary and non-primary areas were relatively robust to simple types of synthetic noise. Our results suggest a general representational transformation between auditory cortical stages, illustrating a representational consequence of hierarchical organization in the auditory system.},
doi = {10.1038/s41467-019-11710-y},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {Mon Sep 02 00:00:00 EDT 2019},
month = {Mon Sep 02 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 18 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Inattentional Deafness: Visual Load Leads to Time-Specific Suppression of Auditory Evoked Responses
journal, December 2015


Rapid Synaptic Depression Explains Nonlinear Modulation of Spectro-Temporal Tuning in Primary Auditory Cortex by Natural Stimuli
journal, March 2009


Control of Attention Shifts between Vision and Audition in Human Cortex
journal, November 2004


Selective Attention in Normal and Impaired Hearing
journal, October 2008


Contribution of spiking activity in the primary auditory cortex to detection in noise
journal, December 2017

  • Christison-Lagay, Kate L.; Bennur, Sharath; Cohen, Yale E.
  • Journal of Neurophysiology, Vol. 118, Issue 6
  • DOI: 10.1152/jn.00521.2017

Identification of a pathway for intelligible speech in the left temporal lobe
journal, December 2000


Statistics of natural reverberation enable perceptual separation of sound and space
journal, November 2016

  • Traer, James; McDermott, Josh H.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
  • DOI: 10.1073/pnas.1612524113

Auditory Processing Disorder and Speech Perception Problems in Noise: Finding the Underlying Origin
journal, June 2010


A Task-Optimized Neural Network Replicates Human Auditory Behavior, Predicts Brain Responses, and Reveals a Cortical Processing Hierarchy
journal, May 2018


Modelling auditory attention
journal, February 2017

  • Kaya, Emine Merve; Elhilali, Mounya
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1714
  • DOI: 10.1098/rstb.2016.0101

Hierarchical Processing of Auditory Objects in Humans
journal, January 2007


Modeling auditory processing of amplitude modulation. I. Detection and masking with narrow-band carriers
journal, November 1997

  • Dau, Torsten; Kollmeier, Birger; Kohlrausch, Armin
  • The Journal of the Acoustical Society of America, Vol. 102, Issue 5
  • DOI: 10.1121/1.420344

Reduction of Information Redundancy in the Ascending Auditory Pathway
journal, August 2006


Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
journal, January 2014


Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI
journal, August 2009

  • Schonwiesner, M.; Zatorre, R. J.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
  • DOI: 10.1073/pnas.0907682106

Processing of complex sounds in the macaque nonprimary auditory cortex
journal, April 1995


Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds
journal, September 2005

  • Woolley, Sarah M. N.; Fremouw, Thane E.; Hsu, Anne
  • Nature Neuroscience, Vol. 8, Issue 10
  • DOI: 10.1038/nn1536

Attentional modulation of human auditory cortex
journal, May 2004

  • Petkov, Christopher I.; Kang, Xiaojian; Alho, Kimmo
  • Nature Neuroscience, Vol. 7, Issue 6
  • DOI: 10.1038/nn1256

Sound Texture Perception via Statistics of the Auditory Periphery: Evidence from Sound Synthesis
journal, September 2011


Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System
journal, April 2001


The cortical analysis of speech-specific temporal structure revealed by responses to sound quilts
journal, May 2015

  • Overath, Tobias; McDermott, Josh H.; Zarate, Jean Mary
  • Nature Neuroscience, Vol. 18, Issue 6
  • DOI: 10.1038/nn.4021

Categorical speech representation in human superior temporal gyrus
journal, October 2010

  • Chang, Edward F.; Rieger, Jochem W.; Johnson, Keith
  • Nature Neuroscience, Vol. 13, Issue 11
  • DOI: 10.1038/nn.2641

Multiple Stages of Auditory Speech Perception Reflected in Event-Related fMRI
journal, December 2006

  • Obleser, J.; Zimmermann, J.; Van Meter, J.
  • Cerebral Cortex, Vol. 17, Issue 10
  • DOI: 10.1093/cercor/bhl133

Modulation spectra of natural sounds and ethological theories of auditory processing
journal, December 2003

  • Singh, Nandini C.; Theunissen, Frédéric E.
  • The Journal of the Acoustical Society of America, Vol. 114, Issue 6
  • DOI: 10.1121/1.1624067

Distinct Cortical Pathways for Music and Speech Revealed by Hypothesis-Free Voxel Decomposition
journal, December 2015


Neural Modulation Tuning Characteristics Scale to Efficiently Encode Natural Sound Statistics
journal, November 2010


Deep neural network models of sensory systems: windows onto the role of task constraints
journal, April 2019


Spectro-Temporal Response Field Characterization With Dynamic Ripples in Ferret Primary Auditory Cortex
journal, March 2001

  • Depireux, Didier A.; Simon, Jonathan Z.; Klein, David J.
  • Journal of Neurophysiology, Vol. 85, Issue 3
  • DOI: 10.1152/jn.2001.85.3.1220

Mechanisms for Allocating Auditory Attention: An Auditory Saliency Map
journal, November 2005

  • Kayser, Christoph; Petkov, Christopher I.; Lippert, Michael
  • Current Biology, Vol. 15, Issue 21
  • DOI: 10.1016/j.cub.2005.09.040

Neural responses to natural and model-matched stimuli reveal distinct computations in primary and nonprimary auditory cortex
journal, December 2018


Nature of Auditory Processing Disorder in Children
journal, July 2010

  • Moore, D. R.; Ferguson, M. A.; Edmondson-Jones, A. M.
  • PEDIATRICS, Vol. 126, Issue 2
  • DOI: 10.1542/peds.2009-2826

Emergence of neural encoding of auditory objects while listening to competing speakers
journal, July 2012

  • Ding, N.; Simon, J. Z.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 29
  • DOI: 10.1073/pnas.1205381109

Contrast Gain Control in Auditory Cortex
journal, June 2011


Perceptual grouping of speech components differing in fundamental frequency and onset-time
journal, May 1981


Constructing Noise-Invariant Representations of Sound in the Auditory Pathway
journal, November 2013


Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates
journal, October 2012

  • Camalier, C. R.; D'Angelo, W. R.; Sterbing-D'Angelo, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 44
  • DOI: 10.1073/pnas.1206387109

Sparse and Background-Invariant Coding of Vocalizations in Auditory Scenes
journal, July 2013


Summary statistics in auditory perception
journal, February 2013

  • McDermott, Josh H.; Schemitsch, Michael; Simoncelli, Eero P.
  • Nature Neuroscience, Vol. 16, Issue 4
  • DOI: 10.1038/nn.3347

Derivation of auditory filter shapes from notched-noise data
journal, August 1990


Normal hearing is not enough to guarantee robust encoding of suprathreshold features important in everyday communication
journal, August 2011

  • Ruggles, D.; Bharadwaj, H.; Shinn-Cunningham, B. G.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 37
  • DOI: 10.1073/pnas.1108912108

Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex
journal, April 2014


Cortical Representations of Speech in a Multitalker Auditory Scene
journal, August 2017


Attentional Selection in a Cocktail Party Environment Can Be Decoded from Single-Trial EEG
journal, January 2014

  • O'Sullivan, James A.; Power, Alan J.; Mesgarani, Nima
  • Cerebral Cortex, Vol. 25, Issue 7
  • DOI: 10.1093/cercor/bht355

Attentive Tracking of Sound Sources
journal, August 2015


Measuring the Performance of Neural Models
journal, February 2016

  • Schoppe, Oliver; Harper, Nicol S.; Willmore, Ben D. B.
  • Frontiers in Computational Neuroscience, Vol. 10
  • DOI: 10.3389/fncom.2016.00010

Functional localization of auditory cortical fields of human: Click-train stimulation
journal, April 2008


The Proof and Measurement of Association between Two Things
journal, January 1904

  • Spearman, C.
  • The American Journal of Psychology, Vol. 15, Issue 1
  • DOI: 10.2307/1412159

Mechanisms of noise robust representation of speech in primary auditory cortex
journal, April 2014

  • Mesgarani, N.; David, S. V.; Fritz, J. B.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 18
  • DOI: 10.1073/pnas.1318017111

Adaptive and Selective Time Averaging of Auditory Scenes
journal, May 2018


Adaptation of the human auditory cortex to changing background noise
journal, June 2019

  • Khalighinejad, Bahar; Herrero, Jose L.; Mehta, Ashesh D.
  • Nature Communications, Vol. 10, Issue 1
  • DOI: 10.1038/s41467-019-10611-4

Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party”
journal, March 2013


Selective cortical representation of attended speaker in multi-talker speech perception
journal, April 2012


Subdivisions of auditory cortex and processing streams in primates
journal, October 2000

  • Kaas, J. H.; Hackett, T. A.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 22
  • DOI: 10.1073/pnas.97.22.11793

Noise-invariant Neurons in the Avian Auditory Cortex: Hearing the Song in Noise
journal, March 2013


Hierarchical Organization of Human Auditory Cortex: Evidence from Acoustic Invariance in the Response to Intelligible Speech
journal, January 2010


Emergence of invariant representation of vocalizations in the auditory cortex
journal, November 2015

  • Carruthers, Isaac M.; Laplagne, Diego A.; Jaegle, Andrew
  • Journal of Neurophysiology, Vol. 114, Issue 5
  • DOI: 10.1152/jn.00095.2015

The neural processing of masked speech
journal, September 2013


Input-Specific Gain Modulation by Local Sensory Context Shapes Cortical and Thalamic Responses to Complex Sounds
journal, July 2016


The proof and measurement of association between two things
journal, October 2010

  • Spearman, C.
  • International Journal of Epidemiology, Vol. 39, Issue 5
  • DOI: 10.1093/ije/dyq191

Hierarchical Processing of Auditory Objects in Humans
journal, January 2005


Paying attention to speech: The role of working memory capacity and professional experience
journal, July 2020

  • Lambez, Bar; Agmon, Galit; Har-Shai Yahav, Paz
  • Attention, Perception, & Psychophysics, Vol. 82, Issue 7
  • DOI: 10.3758/s13414-020-02091-2

The auditory cortex
journal, April 2007


Hierarchical processing of auditory objects in humans
text, January 2007

  • Kumar, S.; Stephan, K. E.; Warren, J. D.
  • Public Library of Science (PLoS)
  • DOI: 10.5167/uzh-50392

The Proof and Measurement of Association between Two Things
journal, October 1987

  • Spearman, C.
  • The American Journal of Psychology, Vol. 100, Issue 3/4
  • DOI: 10.2307/1422689

Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System
journal, April 2001


Deep neural network models of sensory systems: windows onto the role of task constraints
journal, April 2019


Mechanisms for Allocating Auditory Attention: An Auditory Saliency Map
journal, November 2005

  • Kayser, Christoph; Petkov, Christopher I.; Lippert, Michael
  • Current Biology, Vol. 15, Issue 21
  • DOI: 10.1016/j.cub.2005.09.040

Attentive Tracking of Sound Sources
journal, August 2015


Functional localization of auditory cortical fields of human: Click-train stimulation
journal, April 2008


The neural processing of masked speech
journal, September 2013


Reduction of Information Redundancy in the Ascending Auditory Pathway
journal, August 2006


Contrast Gain Control in Auditory Cortex
journal, June 2011


Sound Texture Perception via Statistics of the Auditory Periphery: Evidence from Sound Synthesis
journal, September 2011


Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party”
journal, March 2013


Sparse and Background-Invariant Coding of Vocalizations in Auditory Scenes
journal, July 2013


Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex
journal, April 2014


Functional Convergence of Response Properties in the Auditory Thalamocortical System
journal, October 2001


How AI and neuroscience drive each other forwards
journal, July 2019


Categorical speech representation in human superior temporal gyrus
journal, October 2010

  • Chang, Edward F.; Rieger, Jochem W.; Johnson, Keith
  • Nature Neuroscience, Vol. 13, Issue 11
  • DOI: 10.1038/nn.2641

The cortical analysis of speech-specific temporal structure revealed by responses to sound quilts
journal, May 2015

  • Overath, Tobias; McDermott, Josh H.; Zarate, Jean Mary
  • Nature Neuroscience, Vol. 18, Issue 6
  • DOI: 10.1038/nn.4021

Attentional modulation of human auditory cortex
journal, May 2004

  • Petkov, Christopher I.; Kang, Xiaojian; Alho, Kimmo
  • Nature Neuroscience, Vol. 7, Issue 6
  • DOI: 10.1038/nn1256

Adaptation of the human auditory cortex to changing background noise
journal, June 2019

  • Khalighinejad, Bahar; Herrero, Jose L.; Mehta, Ashesh D.
  • Nature Communications, Vol. 10, Issue 1
  • DOI: 10.1038/s41467-019-10611-4

Slow-to-fast transition of giant creeping rockslides modulated by undrained loading in basal shear zones
journal, March 2020


Auditory Processing Disorder and Speech Perception Problems in Noise: Finding the Underlying Origin
journal, June 2010


Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI
journal, August 2009

  • Schonwiesner, M.; Zatorre, R. J.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
  • DOI: 10.1073/pnas.0907682106

Normal hearing is not enough to guarantee robust encoding of suprathreshold features important in everyday communication
journal, August 2011

  • Ruggles, D.; Bharadwaj, H.; Shinn-Cunningham, B. G.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 37
  • DOI: 10.1073/pnas.1108912108

Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates
journal, October 2012

  • Camalier, C. R.; D'Angelo, W. R.; Sterbing-D'Angelo, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 44
  • DOI: 10.1073/pnas.1206387109

Mechanisms of noise robust representation of speech in primary auditory cortex
journal, April 2014

  • Mesgarani, N.; David, S. V.; Fritz, J. B.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 18
  • DOI: 10.1073/pnas.1318017111

Statistics of natural reverberation enable perceptual separation of sound and space
journal, November 2016

  • Traer, James; McDermott, Josh H.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 48
  • DOI: 10.1073/pnas.1612524113

Subdivisions of auditory cortex and processing streams in primates
journal, October 2000

  • Kaas, J. H.; Hackett, T. A.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 22
  • DOI: 10.1073/pnas.97.22.11793

Perceptual grouping of speech components differing in fundamental frequency and onset-time
journal, May 1981


Identification of a pathway for intelligible speech in the left temporal lobe
journal, December 2000


Multiple Stages of Auditory Speech Perception Reflected in Event-Related fMRI
journal, December 2006

  • Obleser, J.; Zimmermann, J.; Van Meter, J.
  • Cerebral Cortex, Vol. 17, Issue 10
  • DOI: 10.1093/cercor/bhl133

Hierarchical Organization of Human Auditory Cortex: Evidence from Acoustic Invariance in the Response to Intelligible Speech
journal, January 2010


Attentional Selection in a Cocktail Party Environment Can Be Decoded from Single-Trial EEG
journal, January 2014

  • O'Sullivan, James A.; Power, Alan J.; Mesgarani, Nima
  • Cerebral Cortex, Vol. 25, Issue 7
  • DOI: 10.1093/cercor/bht355

Modelling auditory attention
journal, February 2017

  • Kaya, Emine Merve; Elhilali, Mounya
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1714
  • DOI: 10.1098/rstb.2016.0101

Modulation spectra of natural sounds and ethological theories of auditory processing
journal, December 2003

  • Singh, Nandini C.; Theunissen, Frédéric E.
  • The Journal of the Acoustical Society of America, Vol. 114, Issue 6
  • DOI: 10.1121/1.1624067

Modeling auditory processing of amplitude modulation. I. Detection and masking with narrow-band carriers
journal, November 1997

  • Dau, Torsten; Kollmeier, Birger; Kohlrausch, Armin
  • The Journal of the Acoustical Society of America, Vol. 102, Issue 5
  • DOI: 10.1121/1.420344

Emergence of invariant representation of vocalizations in the auditory cortex
journal, November 2015

  • Carruthers, Isaac M.; Laplagne, Diego A.; Jaegle, Andrew
  • Journal of Neurophysiology, Vol. 114, Issue 5
  • DOI: 10.1152/jn.00095.2015

Selective Attention in Normal and Impaired Hearing
journal, October 2008


Hierarchical Processing of Auditory Objects in Humans
journal, January 2007


Hierarchical Processing in Spoken Language Comprehension
journal, April 2003


Level Invariant Representation of Sounds by Populations of Neurons in Primary Auditory Cortex
journal, March 2008


Adding Insult to Injury: Cochlear Nerve Degeneration after "Temporary" Noise-Induced Hearing Loss
journal, November 2009


Musical Experience Limits the Degradative Effects of Background Noise on the Neural Processing of Sound
journal, November 2009


Brain Bases for Auditory Stimulus-Driven Figure-Ground Segregation
journal, January 2011


Adaptive Temporal Encoding Leads to a Background-Insensitive Cortical Representation of Speech
journal, March 2013


Nature of Auditory Processing Disorder in Children
journal, July 2010

  • Moore, D. R.; Ferguson, M. A.; Edmondson-Jones, A. M.
  • PEDIATRICS, Vol. 126, Issue 2
  • DOI: 10.1542/peds.2009-2826

Smooth Granular Sound Texture Synthesis By Control Of Timbral Similarity
text, January 2015


Works referencing / citing this record:

Illusory sound texture reveals multi-second statistical completion in auditory scene analysis
journal, November 2019


EEG-based classification of natural sounds reveals specialized responses to speech and music
journal, April 2020


Illusory sound texture reveals multi-second statistical completion in auditory scene analysis
journal, November 2019