Frequency-specific attentional modulation in human primary auditory cortex and midbrain

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Paying selective attention to an audio frequency selectively enhances activity within primary auditory cortex (PAC) at the tonotopic site (frequency channel) representing that frequency. Animal PAC neurons achieve this 'frequency-specific attentional spotlight' by adapting their frequency tuning, yet comparable evidence in humans is scarce. Moreover, whether the spotlight operates in human midbrain is unknown. To address these issues, we studied the spectral tuning of frequency channels in human PAC and inferior colliculus (IC), using 7-T functional magnetic resonance imaging (FMRI) and frequency mapping, while participants focused on different frequency-specific sounds. We found that shifts in frequency-specific attention alter the response gain, but not tuning profile, of PAC frequency channels. The gain modulation was strongest in low-frequency channels and varied near-monotonically across the tonotopic axis, giving rise to the attentional spotlight. We observed less prominent, non-tonotopic spatial patterns of attentional modulation in IC. These results indicate that the frequency-specific attentional spotlight in human PAC as measured with FMRI arises primarily from tonotopic gain modulation, rather than adapted frequency tuning. Moreover, frequency-specific attentional modulation of afferent sound processing in human IC seems to be considerably weaker, suggesting that the spotlight diminishes toward this lower-order processing stage. Our study sheds light on how the human auditory pathway adapts to the different demands of selective hearing.

Original languageEnglish
Pages (from-to)274-287
Number of pages14
JournalNeuroimage
Volume174
DOIs
Publication statusPublished - 1 Jul 2018

Keywords

  • Journal Article
  • CORTICOFUGAL MODULATION
  • Human primary auditory cortex
  • SUPERIOR TEMPORAL GYRUS
  • Human inferior colliculus
  • Auditory attention
  • SELECTIVE ATTENTION
  • FMRI ACTIVATION
  • BRAIN-STEM
  • SPATIAL ATTENTION
  • TASK-RELATED PLASTICITY
  • INFERIOR COLLICULUS
  • SPECTROTEMPORAL RECEPTIVE-FIELDS
  • Frequency tuning
  • VISUAL-ATTENTION
  • FMRI
  • Humans
  • Male
  • Inferior Colliculi/physiology
  • Young Adult
  • Adult
  • Female
  • Acoustic Stimulation
  • Auditory Perception/physiology
  • Auditory Pathways/physiology
  • Auditory Cortex/physiology
  • Magnetic Resonance Imaging
  • Brain Mapping
  • Attention/physiology

Cite this

@article{c7e4de96494449098a8f97c44e19ca41,
title = "Frequency-specific attentional modulation in human primary auditory cortex and midbrain",
abstract = "Paying selective attention to an audio frequency selectively enhances activity within primary auditory cortex (PAC) at the tonotopic site (frequency channel) representing that frequency. Animal PAC neurons achieve this 'frequency-specific attentional spotlight' by adapting their frequency tuning, yet comparable evidence in humans is scarce. Moreover, whether the spotlight operates in human midbrain is unknown. To address these issues, we studied the spectral tuning of frequency channels in human PAC and inferior colliculus (IC), using 7-T functional magnetic resonance imaging (FMRI) and frequency mapping, while participants focused on different frequency-specific sounds. We found that shifts in frequency-specific attention alter the response gain, but not tuning profile, of PAC frequency channels. The gain modulation was strongest in low-frequency channels and varied near-monotonically across the tonotopic axis, giving rise to the attentional spotlight. We observed less prominent, non-tonotopic spatial patterns of attentional modulation in IC. These results indicate that the frequency-specific attentional spotlight in human PAC as measured with FMRI arises primarily from tonotopic gain modulation, rather than adapted frequency tuning. Moreover, frequency-specific attentional modulation of afferent sound processing in human IC seems to be considerably weaker, suggesting that the spotlight diminishes toward this lower-order processing stage. Our study sheds light on how the human auditory pathway adapts to the different demands of selective hearing.",
keywords = "Journal Article, CORTICOFUGAL MODULATION, Human primary auditory cortex, SUPERIOR TEMPORAL GYRUS, Human inferior colliculus, Auditory attention, SELECTIVE ATTENTION, FMRI ACTIVATION, BRAIN-STEM, SPATIAL ATTENTION, TASK-RELATED PLASTICITY, INFERIOR COLLICULUS, SPECTROTEMPORAL RECEPTIVE-FIELDS, Frequency tuning, VISUAL-ATTENTION, FMRI, Humans, Male, Inferior Colliculi/physiology, Young Adult, Adult, Female, Acoustic Stimulation, Auditory Perception/physiology, Auditory Pathways/physiology, Auditory Cortex/physiology, Magnetic Resonance Imaging, Brain Mapping, Attention/physiology",
author = "Lars Riecke and Peters, {Judith C.} and Giancarlo Valente and Poser, {Benedikt A.} and Kemper, {Valentin G.} and Elia Formisano and Bettina Sorger",
note = "Copyright {\circledC} 2018 The Authors. Published by Elsevier Inc. All rights reserved.",
year = "2018",
month = "7",
day = "1",
doi = "10.1016/j.neuroimage.2018.03.038",
language = "English",
volume = "174",
pages = "274--287",
journal = "Neuroimage",
issn = "1053-8119",
publisher = "Elsevier Science",

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TY - JOUR

T1 - Frequency-specific attentional modulation in human primary auditory cortex and midbrain

AU - Riecke, Lars

AU - Peters, Judith C.

AU - Valente, Giancarlo

AU - Poser, Benedikt A.

AU - Kemper, Valentin G.

AU - Formisano, Elia

AU - Sorger, Bettina

N1 - Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2018/7/1

Y1 - 2018/7/1

N2 - Paying selective attention to an audio frequency selectively enhances activity within primary auditory cortex (PAC) at the tonotopic site (frequency channel) representing that frequency. Animal PAC neurons achieve this 'frequency-specific attentional spotlight' by adapting their frequency tuning, yet comparable evidence in humans is scarce. Moreover, whether the spotlight operates in human midbrain is unknown. To address these issues, we studied the spectral tuning of frequency channels in human PAC and inferior colliculus (IC), using 7-T functional magnetic resonance imaging (FMRI) and frequency mapping, while participants focused on different frequency-specific sounds. We found that shifts in frequency-specific attention alter the response gain, but not tuning profile, of PAC frequency channels. The gain modulation was strongest in low-frequency channels and varied near-monotonically across the tonotopic axis, giving rise to the attentional spotlight. We observed less prominent, non-tonotopic spatial patterns of attentional modulation in IC. These results indicate that the frequency-specific attentional spotlight in human PAC as measured with FMRI arises primarily from tonotopic gain modulation, rather than adapted frequency tuning. Moreover, frequency-specific attentional modulation of afferent sound processing in human IC seems to be considerably weaker, suggesting that the spotlight diminishes toward this lower-order processing stage. Our study sheds light on how the human auditory pathway adapts to the different demands of selective hearing.

AB - Paying selective attention to an audio frequency selectively enhances activity within primary auditory cortex (PAC) at the tonotopic site (frequency channel) representing that frequency. Animal PAC neurons achieve this 'frequency-specific attentional spotlight' by adapting their frequency tuning, yet comparable evidence in humans is scarce. Moreover, whether the spotlight operates in human midbrain is unknown. To address these issues, we studied the spectral tuning of frequency channels in human PAC and inferior colliculus (IC), using 7-T functional magnetic resonance imaging (FMRI) and frequency mapping, while participants focused on different frequency-specific sounds. We found that shifts in frequency-specific attention alter the response gain, but not tuning profile, of PAC frequency channels. The gain modulation was strongest in low-frequency channels and varied near-monotonically across the tonotopic axis, giving rise to the attentional spotlight. We observed less prominent, non-tonotopic spatial patterns of attentional modulation in IC. These results indicate that the frequency-specific attentional spotlight in human PAC as measured with FMRI arises primarily from tonotopic gain modulation, rather than adapted frequency tuning. Moreover, frequency-specific attentional modulation of afferent sound processing in human IC seems to be considerably weaker, suggesting that the spotlight diminishes toward this lower-order processing stage. Our study sheds light on how the human auditory pathway adapts to the different demands of selective hearing.

KW - Journal Article

KW - CORTICOFUGAL MODULATION

KW - Human primary auditory cortex

KW - SUPERIOR TEMPORAL GYRUS

KW - Human inferior colliculus

KW - Auditory attention

KW - SELECTIVE ATTENTION

KW - FMRI ACTIVATION

KW - BRAIN-STEM

KW - SPATIAL ATTENTION

KW - TASK-RELATED PLASTICITY

KW - INFERIOR COLLICULUS

KW - SPECTROTEMPORAL RECEPTIVE-FIELDS

KW - Frequency tuning

KW - VISUAL-ATTENTION

KW - FMRI

KW - Humans

KW - Male

KW - Inferior Colliculi/physiology

KW - Young Adult

KW - Adult

KW - Female

KW - Acoustic Stimulation

KW - Auditory Perception/physiology

KW - Auditory Pathways/physiology

KW - Auditory Cortex/physiology

KW - Magnetic Resonance Imaging

KW - Brain Mapping

KW - Attention/physiology

U2 - 10.1016/j.neuroimage.2018.03.038

DO - 10.1016/j.neuroimage.2018.03.038

M3 - Article

C2 - 29571712

VL - 174

SP - 274

EP - 287

JO - Neuroimage

JF - Neuroimage

SN - 1053-8119

ER -