Keeping track of sound objects in space: The contribution of early-stage auditory areas
The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing path...
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Published in | Hearing research Vol. 366; pp. 17 - 31 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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Elsevier B.V
01.09.2018
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ISSN | 0378-5955 1878-5891 1878-5891 |
DOI | 10.1016/j.heares.2018.03.027 |
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Abstract | The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space.
•7 T fMRI study in normal hearing subjects of repetition effects in early-stage areas.•Stimuli: narrow categories of environmental sounds, lateralized with ITD cues.•Lateral belt areas encode combination of meaning & position of a sound object.•Evidence for position-linked representation of sound objects.•A third auditory stream, with origin in lateral belt, tracks sound objects in space. |
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AbstractList | The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space. The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space. •7 T fMRI study in normal hearing subjects of repetition effects in early-stage areas.•Stimuli: narrow categories of environmental sounds, lateralized with ITD cues.•Lateral belt areas encode combination of meaning & position of a sound object.•Evidence for position-linked representation of sound objects.•A third auditory stream, with origin in lateral belt, tracks sound objects in space. The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space.The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space. |
Author | Crottaz-Herbette, Sonia Clarke, Stephanie Da Costa, Sandra |
Author_xml | – sequence: 1 givenname: Sandra surname: Da Costa fullname: Da Costa, Sandra email: sandra.dacosta@epfl.ch organization: Centre d’Imagerie BioMédicale (CIBM), EPFL et Universités de Lausanne et de Genève, Bâtiment CH, Station 6, CH-1015 Lausanne, Switzerland – sequence: 2 givenname: Stephanie surname: Clarke fullname: Clarke, Stephanie organization: Service de Neuropsychologie et de Neuroréhabilitation, CHUV, Université de Lausanne, Avenue Pierre Decker 5, CH-1011 Lausanne, Switzerland – sequence: 3 givenname: Sonia orcidid: 0000-0003-3944-3952 surname: Crottaz-Herbette fullname: Crottaz-Herbette, Sonia organization: Service de Neuropsychologie et de Neuroréhabilitation, CHUV, Université de Lausanne, Avenue Pierre Decker 5, CH-1011 Lausanne, Switzerland |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29643021$$D View this record in MEDLINE/PubMed |
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Keywords | Three-stream model Sound recognition and localization Early-stage auditory areas Human fMRI Repetition suppression 7T |
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Title | Keeping track of sound objects in space: The contribution of early-stage auditory areas |
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