Egocentric and allocentric representations in auditory cortex

A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which...

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Published inPLoS biology Vol. 15; no. 6; p. e2001878
Main Authors Town, Stephen M., Brimijoin, W. Owen, Bizley, Jennifer K.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 15.06.2017
Public Library of Science (PLoS)
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ISSN1545-7885
1544-9173
1545-7885
DOI10.1371/journal.pbio.2001878

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Abstract A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.
AbstractList A key function of the brain is to provide a stable representation of an object’s location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position. When we hear a sound, we can describe its location relative to ourselves (e.g., “the phone is on my right”) or relative to the world (e.g., “the phone is in the corner”). These descriptions of space are known as egocentric and allocentric, respectively, and illustrate the representation of sound location in reference frames defined either by the observer or the world. We know that neurons in the brain can represent the location of a sound source. However, previous experiments have been performed in static subjects, in which it’s not possible to tell whether spatial tuning reflects sensitivity to the position of the sound relative to the head or in the world. Here, we recorded neurons in the auditory cortex of freely moving ferrets and showed that most cells represent the position of a sound relative to the head, i.e., in an egocentric reference frame. We also recorded a smaller number of allocentric cells that were tuned to the position of a sound in the world, across the movement of the subject. By recording in freely moving animals, we were also able to investigate the neural encoding of sound source distance and the modulation of auditory processing by head movement speed.
A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.
A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.
Audience Academic
Author Bizley, Jennifer K.
Brimijoin, W. Owen
Town, Stephen M.
AuthorAffiliation 1 Ear Institute, University College London, London, United Kingdom
2 MRC/CSO Institute of Hearing Research – Scottish Section, Glasgow, United Kingdom
National Institute of Mental Health, United States of America
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Town SM, Brimijoin WO, Bizley JK (2017) Egocentric and allocentric representations in auditory cortex. PLoS Biol 15(6): e2001878. https://doi.org/10.1371/journal.pbio.2001878
2017 Town et al 2017 Town et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Town SM, Brimijoin WO, Bizley JK (2017) Egocentric and allocentric representations in auditory cortex. PLoS Biol 15(6): e2001878. https://doi.org/10.1371/journal.pbio.2001878
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Town SM, Brimijoin WO, Bizley JK (2017) Egocentric and allocentric representations in auditory cortex. PLoS Biol 15(6): e2001878. https://doi.org/10.1371/journal.pbio.2001878
– notice: 2017 Town et al 2017 Town et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Town SM, Brimijoin WO, Bizley JK (2017) Egocentric and allocentric representations in auditory cortex. PLoS Biol 15(6): e2001878. https://doi.org/10.1371/journal.pbio.2001878
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Snippet A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by...
A key function of the brain is to provide a stable representation of an object’s location in the world. In hearing, sound azimuth and elevation are encoded by...
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StartPage e2001878
SubjectTerms Acoustic Stimulation
Animals
Auditory cortex
Auditory Cortex - cytology
Auditory Cortex - physiology
Auditory Cortex - radiation effects
Auditory system
Behavior, Animal - radiation effects
Biology and Life Sciences
Brain
Coding
Cortex (auditory)
Data collection
Electric Stimulation
Electrodes, Implanted
Electroencephalography
Evoked Potentials, Auditory - radiation effects
Exploratory Behavior - radiation effects
Female
Ferrets
Head
Head movement
Head Movements - radiation effects
Information processing
Localization
Locomotion - radiation effects
Medicine and Health Sciences
Models, Neurological
Models, Psychological
Modulation
Movement
Neural circuitry
Neurons
Neurons - cytology
Neurons - physiology
Neurons - radiation effects
Open source software
Physiological aspects
Position measurement
Representations
Roles
Sound
Sound localization
Sound Localization - radiation effects
Spatial Behavior - radiation effects
Spatial Processing - radiation effects
Tuning
University colleges
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Title Egocentric and allocentric representations in auditory cortex
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http://dx.doi.org/10.1371/journal.pbio.2001878
Volume 15
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