Active sound localization sharpens spatial tuning in human primary auditory cortex

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ("where") processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ("where") task compared with a sound identification ("what") task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements. SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.

Original languageEnglish
Pages (from-to)8574-8587
Number of pages14
JournalJournal of Neuroscience
Volume38
Issue number40
Early online date20 Aug 2018
DOIs
Publication statusPublished - 3 Oct 2018

Keywords

  • Journal Article
  • FIELDS
  • TASK
  • human auditory cortex
  • REPRESENTATION
  • SENSITIVITY
  • NEURAL POPULATIONS
  • MECHANISMS
  • FUNCTIONAL TOPOGRAPHY
  • cortical functional specialization
  • fMRI
  • STREAMS
  • sound localization
  • PLANUM TEMPORALE
  • SOURCE LOCATION

Cite this

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title = "Active sound localization sharpens spatial tuning in human primary auditory cortex",
abstract = "Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ({"}where{"}) processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ({"}where{"}) task compared with a sound identification ({"}what{"}) task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements. SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.",
keywords = "Journal Article, FIELDS, TASK, human auditory cortex, REPRESENTATION, SENSITIVITY, NEURAL POPULATIONS, MECHANISMS, FUNCTIONAL TOPOGRAPHY, cortical functional specialization, fMRI, STREAMS, sound localization, PLANUM TEMPORALE, SOURCE LOCATION",
author = "{van der Heijden}, Kiki and Rauschecker, {Josef P} and Elia Formisano and Giancarlo Valente and {de Gelder}, Beatrice",
note = "Copyright {\circledC} 2018 the authors.",
year = "2018",
month = "10",
day = "3",
doi = "10.1523/JNEUROSCI.0587-18.2018",
language = "English",
volume = "38",
pages = "8574--8587",
journal = "Journal of Neuroscience",
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publisher = "Society for Neuroscience",
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Active sound localization sharpens spatial tuning in human primary auditory cortex. / van der Heijden, Kiki; Rauschecker, Josef P; Formisano, Elia; Valente, Giancarlo; de Gelder, Beatrice.

In: Journal of Neuroscience, Vol. 38, No. 40, 03.10.2018, p. 8574-8587.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Active sound localization sharpens spatial tuning in human primary auditory cortex

AU - van der Heijden, Kiki

AU - Rauschecker, Josef P

AU - Formisano, Elia

AU - Valente, Giancarlo

AU - de Gelder, Beatrice

N1 - Copyright © 2018 the authors.

PY - 2018/10/3

Y1 - 2018/10/3

N2 - Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ("where") processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ("where") task compared with a sound identification ("what") task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements. SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.

AB - Spatial hearing sensitivity in humans is dynamic and task-dependent, but the mechanisms in human auditory cortex that enable dynamic sound location encoding remain unclear. Using functional magnetic resonance imaging (fMRI), we assessed how active behavior affects encoding of sound location (azimuth) in primary auditory cortical areas and planum temporale (PT). According to the hierarchical model of auditory processing and cortical functional specialization, PT is implicated in sound location ("where") processing. Yet, our results show that spatial tuning profiles in primary auditory cortical areas (left primary core and right caudo-medial belt) sharpened during a sound localization ("where") task compared with a sound identification ("what") task. In contrast, spatial tuning in PT was sharp but did not vary with task performance. We further applied a population pattern decoder to the measured fMRI activity patterns, which confirmed the task-dependent effects in the left core: sound location estimates from fMRI patterns measured during active sound localization were most accurate. In PT, decoding accuracy was not modulated by task performance. These results indicate that changes of population activity in human primary auditory areas reflect dynamic and task-dependent processing of sound location. As such, our findings suggest that the hierarchical model of auditory processing may need to be revised to include an interaction between primary and functionally specialized areas depending on behavioral requirements. SIGNIFICANCE STATEMENT According to a purely hierarchical view, cortical auditory processing consists of a series of analysis stages from sensory (acoustic) processing in primary auditory cortex to specialized processing in higher-order areas. Posterior-dorsal cortical auditory areas, planum temporale (PT) in humans, are considered to be functionally specialized for spatial processing. However, this model is based mostly on passive listening studies. Our results provide compelling evidence that active behavior (sound localization) sharpens spatial selectivity in primary auditory cortex, whereas spatial tuning in functionally specialized areas (PT) is narrow but task-invariant. These findings suggest that the hierarchical view of cortical functional specialization needs to be extended: our data indicate that active behavior involves feedback projections from higher-order regions to primary auditory cortex.

KW - Journal Article

KW - FIELDS

KW - TASK

KW - human auditory cortex

KW - REPRESENTATION

KW - SENSITIVITY

KW - NEURAL POPULATIONS

KW - MECHANISMS

KW - FUNCTIONAL TOPOGRAPHY

KW - cortical functional specialization

KW - fMRI

KW - STREAMS

KW - sound localization

KW - PLANUM TEMPORALE

KW - SOURCE LOCATION

U2 - 10.1523/JNEUROSCI.0587-18.2018

DO - 10.1523/JNEUROSCI.0587-18.2018

M3 - Article

C2 - 30126968

VL - 38

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JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

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ER -