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Functional connectivity in the dorsal stream and between bilateral auditory-related cortical areas differentially contribute to speech decoding depending on spectro-temporal signal integrity and performance
Speech processing relies on the interdependence between auditory perception, sensorimotor integration, and verbal memory functions. Functional and structural connectivity between bilateral auditory-related cortical areas (ARCAs) facilitates spectro-temporal analyses, whereas the dynamic interplay be...
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Published in: | Neuropsychologia 2017-11, Vol.106, p.398-406 |
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description | Speech processing relies on the interdependence between auditory perception, sensorimotor integration, and verbal memory functions. Functional and structural connectivity between bilateral auditory-related cortical areas (ARCAs) facilitates spectro-temporal analyses, whereas the dynamic interplay between ARCAs and Broca's area (i.e., dorsal pathway) contributes to verbal memory functions, articulation, and sound-to-motor mapping. However, it remains unclear whether these two neural circuits are preferentially driven by spectral or temporal acoustic information, and whether their recruitment is predictive of speech perception performance and learning. Therefore, we evaluated EEG-based intracranial (eLORETA) functional connectivity (lagged coherence) in both pathways (i.e., between bilateral ARCAs and in the dorsal stream) while good- (GPs, N = 12) and poor performers (PPs, N = 13) learned to decode natural pseudowords (CLEAN) or comparable items (speech-noise chimeras) manipulated in the envelope (ENV) or in the fine-structure (FS). Learning to decode degraded speech was generally associated with increased functional connectivity in the theta, alpha, and beta frequency range in both circuits. Furthermore, GPs exhibited increased connectivity in the left dorsal stream compared to PPs, but only during the FS condition and in the theta frequency band. These results suggest that both pathways contribute to the decoding of spectro-temporal degraded speech by increasing the communication between brain regions involved in perceptual analyses and verbal memory functions. Otherwise, the left-hemispheric recruitment of the dorsal stream in GPs during the FS condition points to a contribution of this pathway to articulatory-based memory processes that are dependent on the temporal integrity of the speech signal. These results enable to better comprehend the neural circuits underlying word-learning as a function of temporal and spectral signal integrity and performance.
•Learning pseudowords manipulated in the envelope or in the fine-structure (FS).•EEG-based functional connectivity in good (GP) and poor performers (PP).•Connectivity in the dorsal stream and between the left and right auditory cortex.•GP exhibited increased connectivity in the left dorsal stream during the FS condition.•Left dorsal connectivity was dependent on the temporal integrity of the speech signal. |
doi_str_mv | 10.1016/j.neuropsychologia.2017.10.030 |
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•Learning pseudowords manipulated in the envelope or in the fine-structure (FS).•EEG-based functional connectivity in good (GP) and poor performers (PP).•Connectivity in the dorsal stream and between the left and right auditory cortex.•GP exhibited increased connectivity in the left dorsal stream during the FS condition.•Left dorsal connectivity was dependent on the temporal integrity of the speech signal.</description><identifier>ISSN: 0028-3932</identifier><identifier>EISSN: 1873-3514</identifier><identifier>DOI: 10.1016/j.neuropsychologia.2017.10.030</identifier><identifier>PMID: 29106999</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adult ; Auditory cortex ; Auditory Cortex - physiology ; Auditory Pathways - physiology ; Broca Area - physiology ; Dorsal stream ; EEG ; Electroencephalography ; Female ; Functional connectivity ; Humans ; Learning - physiology ; Male ; Memory ; Middle Aged ; Noise ; Spectro-temporal processing ; Speech ; Speech learning ; Speech Perception - physiology ; Young Adult</subject><ispartof>Neuropsychologia, 2017-11, Vol.106, p.398-406</ispartof><rights>2017 Elsevier Ltd</rights><rights>Copyright © 2017 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c448t-2442cd400c3e6bc3470ada6bc299595fdd9dd60d9b30f3bbd86d63215ca64a5c3</citedby><cites>FETCH-LOGICAL-c448t-2442cd400c3e6bc3470ada6bc299595fdd9dd60d9b30f3bbd86d63215ca64a5c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29106999$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Elmer, Stefan</creatorcontrib><creatorcontrib>Kühnis, Jürg</creatorcontrib><creatorcontrib>Rauch, Piyush</creatorcontrib><creatorcontrib>Abolfazl Valizadeh, Seyed</creatorcontrib><creatorcontrib>Jäncke, Lutz</creatorcontrib><title>Functional connectivity in the dorsal stream and between bilateral auditory-related cortical areas differentially contribute to speech decoding depending on spectro-temporal signal integrity and performance</title><title>Neuropsychologia</title><addtitle>Neuropsychologia</addtitle><description>Speech processing relies on the interdependence between auditory perception, sensorimotor integration, and verbal memory functions. Functional and structural connectivity between bilateral auditory-related cortical areas (ARCAs) facilitates spectro-temporal analyses, whereas the dynamic interplay between ARCAs and Broca's area (i.e., dorsal pathway) contributes to verbal memory functions, articulation, and sound-to-motor mapping. However, it remains unclear whether these two neural circuits are preferentially driven by spectral or temporal acoustic information, and whether their recruitment is predictive of speech perception performance and learning. Therefore, we evaluated EEG-based intracranial (eLORETA) functional connectivity (lagged coherence) in both pathways (i.e., between bilateral ARCAs and in the dorsal stream) while good- (GPs, N = 12) and poor performers (PPs, N = 13) learned to decode natural pseudowords (CLEAN) or comparable items (speech-noise chimeras) manipulated in the envelope (ENV) or in the fine-structure (FS). Learning to decode degraded speech was generally associated with increased functional connectivity in the theta, alpha, and beta frequency range in both circuits. Furthermore, GPs exhibited increased connectivity in the left dorsal stream compared to PPs, but only during the FS condition and in the theta frequency band. These results suggest that both pathways contribute to the decoding of spectro-temporal degraded speech by increasing the communication between brain regions involved in perceptual analyses and verbal memory functions. Otherwise, the left-hemispheric recruitment of the dorsal stream in GPs during the FS condition points to a contribution of this pathway to articulatory-based memory processes that are dependent on the temporal integrity of the speech signal. These results enable to better comprehend the neural circuits underlying word-learning as a function of temporal and spectral signal integrity and performance.
•Learning pseudowords manipulated in the envelope or in the fine-structure (FS).•EEG-based functional connectivity in good (GP) and poor performers (PP).•Connectivity in the dorsal stream and between the left and right auditory cortex.•GP exhibited increased connectivity in the left dorsal stream during the FS condition.•Left dorsal connectivity was dependent on the temporal integrity of the speech signal.</description><subject>Adult</subject><subject>Auditory cortex</subject><subject>Auditory Cortex - physiology</subject><subject>Auditory Pathways - physiology</subject><subject>Broca Area - physiology</subject><subject>Dorsal stream</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Female</subject><subject>Functional connectivity</subject><subject>Humans</subject><subject>Learning - physiology</subject><subject>Male</subject><subject>Memory</subject><subject>Middle Aged</subject><subject>Noise</subject><subject>Spectro-temporal processing</subject><subject>Speech</subject><subject>Speech learning</subject><subject>Speech Perception - physiology</subject><subject>Young Adult</subject><issn>0028-3932</issn><issn>1873-3514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNqNUUGO1DAQtBCIHRa-gHxCXDLYcZKJL0hoxbJIK3GBs-XYnRmPEju0nUX5JG_CZhYOnDi57aquancR8oazPWe8e3fee1gxLHEzpzCFo9P7mvFDBvdMsCdkx_uDqETLm6dkx1jdV0KK-oq8iPHMGGvaun9OrmrJWSel3JGft6s3yQWvJ2qC95AvDy5t1HmaTkBtwJihmBD0TLW3dID0A8DTwU06AWZQr9algFuFUJ5sFsLkTEFyV6TWjSMg-OT0NG3FJqEb1gQ0BRoXAHOiFkywzh9zsYD_XQVfQJMwVAnmJRSr6I5lUucTHLGMWSZaAMeAs_YGXpJno54ivHo8r8m3249fb-6q-y-fPt98uK9M0_SpqpumNrZhzAjoBiOaA9NW56qWspXtaK20tmNWDoKNYhhs39lO1Lw1umt0a8Q1eXvRXTB8XyEmNbtoYJq0h7BGxWXHO3EQgmfq-wvVYIgRYVQLulnjpjhTJVN1Vv9mqkqmBc-ZZoHXj17rMIP92_4nxEy4uxAg__jBAapoHORtWId5f8oG979evwBRqMYH</recordid><startdate>201711</startdate><enddate>201711</enddate><creator>Elmer, Stefan</creator><creator>Kühnis, Jürg</creator><creator>Rauch, Piyush</creator><creator>Abolfazl Valizadeh, Seyed</creator><creator>Jäncke, Lutz</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201711</creationdate><title>Functional connectivity in the dorsal stream and between bilateral auditory-related cortical areas differentially contribute to speech decoding depending on spectro-temporal signal integrity and performance</title><author>Elmer, Stefan ; Kühnis, Jürg ; Rauch, Piyush ; Abolfazl Valizadeh, Seyed ; Jäncke, Lutz</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c448t-2442cd400c3e6bc3470ada6bc299595fdd9dd60d9b30f3bbd86d63215ca64a5c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adult</topic><topic>Auditory cortex</topic><topic>Auditory Cortex - physiology</topic><topic>Auditory Pathways - physiology</topic><topic>Broca Area - physiology</topic><topic>Dorsal stream</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Female</topic><topic>Functional connectivity</topic><topic>Humans</topic><topic>Learning - physiology</topic><topic>Male</topic><topic>Memory</topic><topic>Middle Aged</topic><topic>Noise</topic><topic>Spectro-temporal processing</topic><topic>Speech</topic><topic>Speech learning</topic><topic>Speech Perception - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Elmer, Stefan</creatorcontrib><creatorcontrib>Kühnis, Jürg</creatorcontrib><creatorcontrib>Rauch, Piyush</creatorcontrib><creatorcontrib>Abolfazl Valizadeh, Seyed</creatorcontrib><creatorcontrib>Jäncke, Lutz</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Neuropsychologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Elmer, Stefan</au><au>Kühnis, Jürg</au><au>Rauch, Piyush</au><au>Abolfazl Valizadeh, Seyed</au><au>Jäncke, Lutz</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional connectivity in the dorsal stream and between bilateral auditory-related cortical areas differentially contribute to speech decoding depending on spectro-temporal signal integrity and performance</atitle><jtitle>Neuropsychologia</jtitle><addtitle>Neuropsychologia</addtitle><date>2017-11</date><risdate>2017</risdate><volume>106</volume><spage>398</spage><epage>406</epage><pages>398-406</pages><issn>0028-3932</issn><eissn>1873-3514</eissn><abstract>Speech processing relies on the interdependence between auditory perception, sensorimotor integration, and verbal memory functions. Functional and structural connectivity between bilateral auditory-related cortical areas (ARCAs) facilitates spectro-temporal analyses, whereas the dynamic interplay between ARCAs and Broca's area (i.e., dorsal pathway) contributes to verbal memory functions, articulation, and sound-to-motor mapping. However, it remains unclear whether these two neural circuits are preferentially driven by spectral or temporal acoustic information, and whether their recruitment is predictive of speech perception performance and learning. Therefore, we evaluated EEG-based intracranial (eLORETA) functional connectivity (lagged coherence) in both pathways (i.e., between bilateral ARCAs and in the dorsal stream) while good- (GPs, N = 12) and poor performers (PPs, N = 13) learned to decode natural pseudowords (CLEAN) or comparable items (speech-noise chimeras) manipulated in the envelope (ENV) or in the fine-structure (FS). Learning to decode degraded speech was generally associated with increased functional connectivity in the theta, alpha, and beta frequency range in both circuits. Furthermore, GPs exhibited increased connectivity in the left dorsal stream compared to PPs, but only during the FS condition and in the theta frequency band. These results suggest that both pathways contribute to the decoding of spectro-temporal degraded speech by increasing the communication between brain regions involved in perceptual analyses and verbal memory functions. Otherwise, the left-hemispheric recruitment of the dorsal stream in GPs during the FS condition points to a contribution of this pathway to articulatory-based memory processes that are dependent on the temporal integrity of the speech signal. These results enable to better comprehend the neural circuits underlying word-learning as a function of temporal and spectral signal integrity and performance.
•Learning pseudowords manipulated in the envelope or in the fine-structure (FS).•EEG-based functional connectivity in good (GP) and poor performers (PP).•Connectivity in the dorsal stream and between the left and right auditory cortex.•GP exhibited increased connectivity in the left dorsal stream during the FS condition.•Left dorsal connectivity was dependent on the temporal integrity of the speech signal.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>29106999</pmid><doi>10.1016/j.neuropsychologia.2017.10.030</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adult Auditory cortex Auditory Cortex - physiology Auditory Pathways - physiology Broca Area - physiology Dorsal stream EEG Electroencephalography Female Functional connectivity Humans Learning - physiology Male Memory Middle Aged Noise Spectro-temporal processing Speech Speech learning Speech Perception - physiology Young Adult |
title | Functional connectivity in the dorsal stream and between bilateral auditory-related cortical areas differentially contribute to speech decoding depending on spectro-temporal signal integrity and performance |
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