Brief Stimulus Exposure Fully Remediates Temporal Processing Deficits Induced by Early Hearing Loss
In childhood, partial hearing loss can produce prolonged deficits in speech perception and temporal processing. However, early therapeutic interventions targeting temporal processing may improve later speech-related outcomes. Gap detection is a measure of auditory temporal resolution that relies on...
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description | In childhood, partial hearing loss can produce prolonged deficits in speech perception and temporal processing. However, early therapeutic interventions targeting temporal processing may improve later speech-related outcomes. Gap detection is a measure of auditory temporal resolution that relies on the auditory cortex (ACx), and early auditory deprivation alters intrinsic and synaptic properties in the ACx. Thus, early deprivation should induce deficits in gap detection, which should be reflected in ACx gap sensitivity. We tested whether earplugging-induced, early transient auditory deprivation in male and female Mongolian gerbils caused correlated deficits in behavioral and cortical gap detection, and whether these could be rescued by a novel therapeutic approach: brief exposure to gaps in background noise. Two weeks after earplug removal, animals that had been earplugged from hearing onset throughout auditory critical periods displayed impaired behavioral gap detection thresholds (GDTs), but this deficit was fully reversed by three 1 h sessions of exposure to gaps in noise. In parallel, after earplugging, cortical GDTs increased because fewer cells were sensitive to short gaps, and gap exposure normalized this pattern. Furthermore, in deprived animals, both first-spike latency and first-spike latency jitter increased, while spontaneous and evoked firing rates decreased, suggesting that deprivation causes a wider range of perceptual problems than measured here. These cortical changes all returned to control levels after gap exposure. Thus, brief stimulus exposure, perhaps in a salient context such as the unfamiliar placement into a testing apparatus, rescued impaired gap detection and may have potential as a remediation tool for general auditory processing deficits.
Hearing loss in early childhood leads to impairments in auditory perception and language processing that can last well beyond the restoration of hearing sensitivity. Perceptual deficits can be improved by training, or by acoustic enrichment in animal models, but both approaches involve extended time and effort. Here, we used a novel remediation technique, brief periods of auditory stimulus exposure, to fully remediate cortical and perceptual deficits in gap detection induced by early transient hearing loss. This technique also improved multiple cortical response properties. Rescue by this efficient exposure regime may have potential as a therapeutic tool to remediate general auditory processin |
doi_str_mv | 10.1523/JNEUROSCI.0916-17.2017 |
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Hearing loss in early childhood leads to impairments in auditory perception and language processing that can last well beyond the restoration of hearing sensitivity. Perceptual deficits can be improved by training, or by acoustic enrichment in animal models, but both approaches involve extended time and effort. Here, we used a novel remediation technique, brief periods of auditory stimulus exposure, to fully remediate cortical and perceptual deficits in gap detection induced by early transient hearing loss. This technique also improved multiple cortical response properties. Rescue by this efficient exposure regime may have potential as a therapeutic tool to remediate general auditory processing deficits in children with perceptual challenges arising from early hearing loss.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0916-17.2017</identifier><identifier>PMID: 28706081</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Acoustic Stimulation - methods ; Age Factors ; Animals ; Auditory Cortex - physiology ; Auditory Cortex - physiopathology ; Auditory deprivation ; Auditory Perception - physiology ; Background noise ; Children ; Cortex (auditory) ; Cortex (temporal) ; Deprivation ; Evoked Potentials, Auditory, Brain Stem - physiology ; Exposure ; Female ; Gerbillinae ; Hearing loss ; Hearing Loss - physiopathology ; Information processing ; Latency ; Male ; Noise ; Speech perception ; Temporal resolution ; Test equipment ; Therapeutic applications ; Vibration</subject><ispartof>The Journal of neuroscience, 2017-08, Vol.37 (32), p.7759-7771</ispartof><rights>Copyright © 2017 the authors 0270-6474/17/377759-13$15.00/0.</rights><rights>Copyright Society for Neuroscience Aug 9, 2017</rights><rights>Copyright © 2017 the authors 0270-6474/17/377759-13$15.00/0 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-c9c63df8b46f6279d8809ae8444adaeb6ea6326d2949eea3b1883924ce8af4013</citedby><orcidid>0000-0001-9832-3075 ; 0000-0002-1973-2207</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5551066/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5551066/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28706081$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Green, David B</creatorcontrib><creatorcontrib>Mattingly, Michelle M</creatorcontrib><creatorcontrib>Ye, Yi</creatorcontrib><creatorcontrib>Gay, Jennifer D</creatorcontrib><creatorcontrib>Rosen, Merri J</creatorcontrib><title>Brief Stimulus Exposure Fully Remediates Temporal Processing Deficits Induced by Early Hearing Loss</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>In childhood, partial hearing loss can produce prolonged deficits in speech perception and temporal processing. However, early therapeutic interventions targeting temporal processing may improve later speech-related outcomes. Gap detection is a measure of auditory temporal resolution that relies on the auditory cortex (ACx), and early auditory deprivation alters intrinsic and synaptic properties in the ACx. Thus, early deprivation should induce deficits in gap detection, which should be reflected in ACx gap sensitivity. We tested whether earplugging-induced, early transient auditory deprivation in male and female Mongolian gerbils caused correlated deficits in behavioral and cortical gap detection, and whether these could be rescued by a novel therapeutic approach: brief exposure to gaps in background noise. Two weeks after earplug removal, animals that had been earplugged from hearing onset throughout auditory critical periods displayed impaired behavioral gap detection thresholds (GDTs), but this deficit was fully reversed by three 1 h sessions of exposure to gaps in noise. In parallel, after earplugging, cortical GDTs increased because fewer cells were sensitive to short gaps, and gap exposure normalized this pattern. Furthermore, in deprived animals, both first-spike latency and first-spike latency jitter increased, while spontaneous and evoked firing rates decreased, suggesting that deprivation causes a wider range of perceptual problems than measured here. These cortical changes all returned to control levels after gap exposure. Thus, brief stimulus exposure, perhaps in a salient context such as the unfamiliar placement into a testing apparatus, rescued impaired gap detection and may have potential as a remediation tool for general auditory processing deficits.
Hearing loss in early childhood leads to impairments in auditory perception and language processing that can last well beyond the restoration of hearing sensitivity. Perceptual deficits can be improved by training, or by acoustic enrichment in animal models, but both approaches involve extended time and effort. Here, we used a novel remediation technique, brief periods of auditory stimulus exposure, to fully remediate cortical and perceptual deficits in gap detection induced by early transient hearing loss. This technique also improved multiple cortical response properties. Rescue by this efficient exposure regime may have potential as a therapeutic tool to remediate general auditory processing deficits in children with perceptual challenges arising from early hearing loss.</description><subject>Acoustic Stimulation - methods</subject><subject>Age Factors</subject><subject>Animals</subject><subject>Auditory Cortex - physiology</subject><subject>Auditory Cortex - physiopathology</subject><subject>Auditory deprivation</subject><subject>Auditory Perception - physiology</subject><subject>Background noise</subject><subject>Children</subject><subject>Cortex (auditory)</subject><subject>Cortex (temporal)</subject><subject>Deprivation</subject><subject>Evoked Potentials, Auditory, Brain Stem - physiology</subject><subject>Exposure</subject><subject>Female</subject><subject>Gerbillinae</subject><subject>Hearing loss</subject><subject>Hearing Loss - physiopathology</subject><subject>Information processing</subject><subject>Latency</subject><subject>Male</subject><subject>Noise</subject><subject>Speech perception</subject><subject>Temporal resolution</subject><subject>Test equipment</subject><subject>Therapeutic applications</subject><subject>Vibration</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUtv1DAUhS0EokPhL1SW2LDJ4Fcce4MEw5QOGlHUx9pynJviKomndoyYf49HLSNg5cX9zvG59yB0RsmS1oy___ptfXt1eb3aLImmsqLNkhHaPEOLMtUVE4Q-RwvCGlJJ0YgT9Cqle0JIU6CX6ISphkii6AK5T9FDj69nP-YhJ7z-tQspR8DneRj2-ApG6LydIeEbGHch2gF_j8FBSn66w5-h987PCW-mLjvocLvHaxuL8AJsPBDbkNJr9KK3Q4I3T-8puj1f36wuqu3ll83q47ZyQrC5ctpJ3vWqFbKXrNGdUkRbUEII21loJVjJmeyYFhrA8pYqxTUTDpTty8L8FH149N3ltsR2MM0lr9lFP9q4N8F68-9k8j_MXfhp6rqmRMpi8O7JIIaHDGk2o08OhsFOEHIyVJcjlx8pL-jb_9D7kONU1jOMaCE0l7QulHykXCx3iNAfw1BiDj2aY4_m0KOhjTn0WIRnf69ylP0pjv8G8fSbiw</recordid><startdate>20170809</startdate><enddate>20170809</enddate><creator>Green, David B</creator><creator>Mattingly, Michelle M</creator><creator>Ye, Yi</creator><creator>Gay, Jennifer D</creator><creator>Rosen, Merri J</creator><general>Society for Neuroscience</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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9832-3075</orcidid><orcidid>https://orcid.org/0000-0002-1973-2207</orcidid></search><sort><creationdate>20170809</creationdate><title>Brief Stimulus Exposure Fully Remediates Temporal Processing Deficits Induced by Early Hearing Loss</title><author>Green, David B ; Mattingly, Michelle M ; Ye, Yi ; Gay, Jennifer D ; Rosen, Merri J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-c9c63df8b46f6279d8809ae8444adaeb6ea6326d2949eea3b1883924ce8af4013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acoustic Stimulation - methods</topic><topic>Age Factors</topic><topic>Animals</topic><topic>Auditory Cortex - physiology</topic><topic>Auditory Cortex - physiopathology</topic><topic>Auditory deprivation</topic><topic>Auditory Perception - physiology</topic><topic>Background noise</topic><topic>Children</topic><topic>Cortex (auditory)</topic><topic>Cortex (temporal)</topic><topic>Deprivation</topic><topic>Evoked Potentials, Auditory, Brain Stem - physiology</topic><topic>Exposure</topic><topic>Female</topic><topic>Gerbillinae</topic><topic>Hearing loss</topic><topic>Hearing Loss - physiopathology</topic><topic>Information processing</topic><topic>Latency</topic><topic>Male</topic><topic>Noise</topic><topic>Speech perception</topic><topic>Temporal resolution</topic><topic>Test equipment</topic><topic>Therapeutic applications</topic><topic>Vibration</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Green, David B</creatorcontrib><creatorcontrib>Mattingly, Michelle M</creatorcontrib><creatorcontrib>Ye, Yi</creatorcontrib><creatorcontrib>Gay, Jennifer D</creatorcontrib><creatorcontrib>Rosen, Merri J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Green, David B</au><au>Mattingly, Michelle M</au><au>Ye, Yi</au><au>Gay, Jennifer D</au><au>Rosen, Merri J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brief Stimulus Exposure Fully Remediates Temporal Processing Deficits Induced by Early Hearing Loss</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2017-08-09</date><risdate>2017</risdate><volume>37</volume><issue>32</issue><spage>7759</spage><epage>7771</epage><pages>7759-7771</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>In childhood, partial hearing loss can produce prolonged deficits in speech perception and temporal processing. However, early therapeutic interventions targeting temporal processing may improve later speech-related outcomes. Gap detection is a measure of auditory temporal resolution that relies on the auditory cortex (ACx), and early auditory deprivation alters intrinsic and synaptic properties in the ACx. Thus, early deprivation should induce deficits in gap detection, which should be reflected in ACx gap sensitivity. We tested whether earplugging-induced, early transient auditory deprivation in male and female Mongolian gerbils caused correlated deficits in behavioral and cortical gap detection, and whether these could be rescued by a novel therapeutic approach: brief exposure to gaps in background noise. Two weeks after earplug removal, animals that had been earplugged from hearing onset throughout auditory critical periods displayed impaired behavioral gap detection thresholds (GDTs), but this deficit was fully reversed by three 1 h sessions of exposure to gaps in noise. In parallel, after earplugging, cortical GDTs increased because fewer cells were sensitive to short gaps, and gap exposure normalized this pattern. Furthermore, in deprived animals, both first-spike latency and first-spike latency jitter increased, while spontaneous and evoked firing rates decreased, suggesting that deprivation causes a wider range of perceptual problems than measured here. These cortical changes all returned to control levels after gap exposure. Thus, brief stimulus exposure, perhaps in a salient context such as the unfamiliar placement into a testing apparatus, rescued impaired gap detection and may have potential as a remediation tool for general auditory processing deficits.
Hearing loss in early childhood leads to impairments in auditory perception and language processing that can last well beyond the restoration of hearing sensitivity. Perceptual deficits can be improved by training, or by acoustic enrichment in animal models, but both approaches involve extended time and effort. Here, we used a novel remediation technique, brief periods of auditory stimulus exposure, to fully remediate cortical and perceptual deficits in gap detection induced by early transient hearing loss. This technique also improved multiple cortical response properties. Rescue by this efficient exposure regime may have potential as a therapeutic tool to remediate general auditory processing deficits in children with perceptual challenges arising from early hearing loss.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>28706081</pmid><doi>10.1523/JNEUROSCI.0916-17.2017</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-9832-3075</orcidid><orcidid>https://orcid.org/0000-0002-1973-2207</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic Stimulation - methods Age Factors Animals Auditory Cortex - physiology Auditory Cortex - physiopathology Auditory deprivation Auditory Perception - physiology Background noise Children Cortex (auditory) Cortex (temporal) Deprivation Evoked Potentials, Auditory, Brain Stem - physiology Exposure Female Gerbillinae Hearing loss Hearing Loss - physiopathology Information processing Latency Male Noise Speech perception Temporal resolution Test equipment Therapeutic applications Vibration |
title | Brief Stimulus Exposure Fully Remediates Temporal Processing Deficits Induced by Early Hearing Loss |
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