Multi-sensory integration in brainstem and auditory cortex
Abstract Tinnitus is the perception of sound in the absence of a physical sound stimulus. It is thought to arise from aberrant neural activity within central auditory pathways that may be influenced by multiple brain centers, including the somatosensory system. Auditory–somatosensory (bimodal) integ...
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description | Abstract Tinnitus is the perception of sound in the absence of a physical sound stimulus. It is thought to arise from aberrant neural activity within central auditory pathways that may be influenced by multiple brain centers, including the somatosensory system. Auditory–somatosensory (bimodal) integration occurs in the dorsal cochlear nucleus (DCN), where electrical activation of somatosensory regions alters pyramidal cell spike timing and rates of sound stimuli. Moreover, in conditions of tinnitus, bimodal integration in DCN is enhanced, producing greater spontaneous and sound-driven neural activity, which are neural correlates of tinnitus. In primary auditory cortex (A1), a similar auditory–somatosensory integration has been described in the normal system (Lakatos et al., 2007), where sub-threshold multisensory modulation may be a direct reflection of subcortical multisensory responses (Tyll et al., 2011). The present work utilized simultaneous recordings from both DCN and A1 to directly compare bimodal integration across these separate brain stations of the intact auditory pathway. Four-shank, 32-channel electrodes were placed in DCN and A1 to simultaneously record tone-evoked unit activity in the presence and absence of spinal trigeminal nucleus (Sp5) electrical activation. Bimodal stimulation led to long-lasting facilitation or suppression of single and multi-unit responses to subsequent sound in both DCN and A1. Immediate (bimodal response) and long-lasting (bimodal plasticity) effects of Sp5-tone stimulation were facilitation or suppression of tone-evoked firing rates in DCN and A1 at all Sp5-tone pairing intervals (10, 20, and 40 ms), and greater suppression at 20 ms pairing-intervals for single unit responses. Understanding the complex relationships between DCN and A1 bimodal processing in the normal animal provides the basis for studying its disruption in hearing loss and tinnitus models. This article is part of a Special Issue entitled: Tinnitus Neuroscience. |
doi_str_mv | 10.1016/j.brainres.2012.08.037 |
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It is thought to arise from aberrant neural activity within central auditory pathways that may be influenced by multiple brain centers, including the somatosensory system. Auditory–somatosensory (bimodal) integration occurs in the dorsal cochlear nucleus (DCN), where electrical activation of somatosensory regions alters pyramidal cell spike timing and rates of sound stimuli. Moreover, in conditions of tinnitus, bimodal integration in DCN is enhanced, producing greater spontaneous and sound-driven neural activity, which are neural correlates of tinnitus. In primary auditory cortex (A1), a similar auditory–somatosensory integration has been described in the normal system (Lakatos et al., 2007), where sub-threshold multisensory modulation may be a direct reflection of subcortical multisensory responses (Tyll et al., 2011). The present work utilized simultaneous recordings from both DCN and A1 to directly compare bimodal integration across these separate brain stations of the intact auditory pathway. Four-shank, 32-channel electrodes were placed in DCN and A1 to simultaneously record tone-evoked unit activity in the presence and absence of spinal trigeminal nucleus (Sp5) electrical activation. Bimodal stimulation led to long-lasting facilitation or suppression of single and multi-unit responses to subsequent sound in both DCN and A1. Immediate (bimodal response) and long-lasting (bimodal plasticity) effects of Sp5-tone stimulation were facilitation or suppression of tone-evoked firing rates in DCN and A1 at all Sp5-tone pairing intervals (10, 20, and 40 ms), and greater suppression at 20 ms pairing-intervals for single unit responses. Understanding the complex relationships between DCN and A1 bimodal processing in the normal animal provides the basis for studying its disruption in hearing loss and tinnitus models. 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It is thought to arise from aberrant neural activity within central auditory pathways that may be influenced by multiple brain centers, including the somatosensory system. Auditory–somatosensory (bimodal) integration occurs in the dorsal cochlear nucleus (DCN), where electrical activation of somatosensory regions alters pyramidal cell spike timing and rates of sound stimuli. Moreover, in conditions of tinnitus, bimodal integration in DCN is enhanced, producing greater spontaneous and sound-driven neural activity, which are neural correlates of tinnitus. In primary auditory cortex (A1), a similar auditory–somatosensory integration has been described in the normal system (Lakatos et al., 2007), where sub-threshold multisensory modulation may be a direct reflection of subcortical multisensory responses (Tyll et al., 2011). The present work utilized simultaneous recordings from both DCN and A1 to directly compare bimodal integration across these separate brain stations of the intact auditory pathway. Four-shank, 32-channel electrodes were placed in DCN and A1 to simultaneously record tone-evoked unit activity in the presence and absence of spinal trigeminal nucleus (Sp5) electrical activation. Bimodal stimulation led to long-lasting facilitation or suppression of single and multi-unit responses to subsequent sound in both DCN and A1. Immediate (bimodal response) and long-lasting (bimodal plasticity) effects of Sp5-tone stimulation were facilitation or suppression of tone-evoked firing rates in DCN and A1 at all Sp5-tone pairing intervals (10, 20, and 40 ms), and greater suppression at 20 ms pairing-intervals for single unit responses. Understanding the complex relationships between DCN and A1 bimodal processing in the normal animal provides the basis for studying its disruption in hearing loss and tinnitus models. This article is part of a Special Issue entitled: Tinnitus Neuroscience.</description><subject>Acoustic Stimulation</subject><subject>Animals</subject><subject>Auditory Cortex - chemistry</subject><subject>Auditory Cortex - physiology</subject><subject>Auditory pathways</subject><subject>Auditory Perception - physiology</subject><subject>Bimodal integration</subject><subject>Brain</subject><subject>Brain stem</subject><subject>Brain Stem - chemistry</subject><subject>Brain Stem - physiology</subject><subject>Cochlear nuclei</subject><subject>Cochlear Nucleus - physiology</subject><subject>cortex</subject><subject>Cortex (auditory)</subject><subject>Cortex (somatosensory)</subject><subject>Data Interpretation, Statistical</subject><subject>Dorsal cochlear nucleus</subject><subject>Electric Stimulation</subject><subject>Electrodes</subject><subject>Electrophysiological Phenomena</subject><subject>Female</subject><subject>Firing pattern</subject><subject>Firing rate</subject><subject>Guinea Pigs</subject><subject>hearing</subject><subject>Hearing loss</subject><subject>Integration</subject><subject>Nervous system</subject><subject>Neurology</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons - physiology</subject><subject>Perception</subject><subject>Physical Stimulation</subject><subject>Primary auditory cortex</subject><subject>Pyramidal cells</subject><subject>Sensory integration</subject><subject>Somatosensory</subject><subject>Somatosensory system</subject><subject>Spinal trigeminal nucleus</subject><subject>Tinnitus</subject><subject>Tinnitus - physiopathology</subject><subject>Trigeminal Nuclei - physiology</subject><subject>Unit activity</subject><issn>0006-8993</issn><issn>1872-6240</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk9v1DAQxS0EokvhK5Q9csnif3FsDhVVRQGpiEPpeeQ4k8VL1i52UrHfvk63rYDLnmzLv3l-4zeEnDC6YpSp95tVm6wPCfOKU8ZXVK-oaJ6RBdMNrxSX9DlZUEpVpY0RR-RVzptyFMLQl-SIc2PqWtYL8uHbNIy-yhhyTLulDyOukx19DGW_vH8jj7hd2tAt7dT5caZcTCP-eU1e9HbI-OZhPSbXF59-nH-pLr9__np-dlk5pflYta7tUWnNjWqd5VL0qK3B1hmne9bVlvIeO2tcZ9AqRk07uzdSmq5taG3EMTnd695M7RY7h2FMdoCb5Lc27SBaD__eBP8T1vEWhCy9N7QIvHsQSPH3hHmErc8Oh8EGjFMGJmSjqZZUHkZZw3T5untbh1BhFFNG8oKqPepSzDlh_2SeUZjjhA08xglznEA1lDhL4cnfrT-VPeZXgLd7oLcR7Dr5DNdXRaEuWRup9Nz8xz2BJaJbjwmy8xgcdj6hG6GL_rCL0_8k3OCDd3b4hTvMmzilUAYAGORSA1fz2M1Tx4qIMOUf7gBXVNPY</recordid><startdate>20121116</startdate><enddate>20121116</enddate><creator>Basura, Gregory J</creator><creator>Koehler, Seth D</creator><creator>Shore, Susan E</creator><general>Elsevier B.V</general><scope>FBQ</scope><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><scope>7TK</scope><scope>7T9</scope><scope>5PM</scope></search><sort><creationdate>20121116</creationdate><title>Multi-sensory integration in brainstem and auditory cortex</title><author>Basura, Gregory J ; Koehler, Seth D ; Shore, Susan E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c682t-bcbfe688296bca243fe8a9ebc9c8f1d5a02feda9cd9ea6109b62409449db70593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Acoustic Stimulation</topic><topic>Animals</topic><topic>Auditory Cortex - chemistry</topic><topic>Auditory Cortex - physiology</topic><topic>Auditory pathways</topic><topic>Auditory Perception - physiology</topic><topic>Bimodal integration</topic><topic>Brain</topic><topic>Brain stem</topic><topic>Brain Stem - chemistry</topic><topic>Brain Stem - physiology</topic><topic>Cochlear nuclei</topic><topic>Cochlear Nucleus - physiology</topic><topic>cortex</topic><topic>Cortex (auditory)</topic><topic>Cortex (somatosensory)</topic><topic>Data Interpretation, Statistical</topic><topic>Dorsal cochlear nucleus</topic><topic>Electric Stimulation</topic><topic>Electrodes</topic><topic>Electrophysiological Phenomena</topic><topic>Female</topic><topic>Firing pattern</topic><topic>Firing rate</topic><topic>Guinea Pigs</topic><topic>hearing</topic><topic>Hearing loss</topic><topic>Integration</topic><topic>Nervous system</topic><topic>Neurology</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons - physiology</topic><topic>Perception</topic><topic>Physical Stimulation</topic><topic>Primary auditory cortex</topic><topic>Pyramidal cells</topic><topic>Sensory integration</topic><topic>Somatosensory</topic><topic>Somatosensory system</topic><topic>Spinal trigeminal nucleus</topic><topic>Tinnitus</topic><topic>Tinnitus - physiopathology</topic><topic>Trigeminal Nuclei - physiology</topic><topic>Unit activity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Basura, Gregory J</creatorcontrib><creatorcontrib>Koehler, Seth D</creatorcontrib><creatorcontrib>Shore, Susan E</creatorcontrib><collection>AGRIS</collection><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><collection>Neurosciences Abstracts</collection><collection>Linguistics and Language Behavior Abstracts (LLBA)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Brain research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Basura, Gregory J</au><au>Koehler, Seth D</au><au>Shore, Susan E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multi-sensory integration in brainstem and auditory cortex</atitle><jtitle>Brain research</jtitle><addtitle>Brain Res</addtitle><date>2012-11-16</date><risdate>2012</risdate><volume>1485</volume><issue>Nov 16</issue><spage>95</spage><epage>107</epage><pages>95-107</pages><issn>0006-8993</issn><eissn>1872-6240</eissn><abstract>Abstract Tinnitus is the perception of sound in the absence of a physical sound stimulus. It is thought to arise from aberrant neural activity within central auditory pathways that may be influenced by multiple brain centers, including the somatosensory system. Auditory–somatosensory (bimodal) integration occurs in the dorsal cochlear nucleus (DCN), where electrical activation of somatosensory regions alters pyramidal cell spike timing and rates of sound stimuli. Moreover, in conditions of tinnitus, bimodal integration in DCN is enhanced, producing greater spontaneous and sound-driven neural activity, which are neural correlates of tinnitus. In primary auditory cortex (A1), a similar auditory–somatosensory integration has been described in the normal system (Lakatos et al., 2007), where sub-threshold multisensory modulation may be a direct reflection of subcortical multisensory responses (Tyll et al., 2011). The present work utilized simultaneous recordings from both DCN and A1 to directly compare bimodal integration across these separate brain stations of the intact auditory pathway. Four-shank, 32-channel electrodes were placed in DCN and A1 to simultaneously record tone-evoked unit activity in the presence and absence of spinal trigeminal nucleus (Sp5) electrical activation. Bimodal stimulation led to long-lasting facilitation or suppression of single and multi-unit responses to subsequent sound in both DCN and A1. Immediate (bimodal response) and long-lasting (bimodal plasticity) effects of Sp5-tone stimulation were facilitation or suppression of tone-evoked firing rates in DCN and A1 at all Sp5-tone pairing intervals (10, 20, and 40 ms), and greater suppression at 20 ms pairing-intervals for single unit responses. Understanding the complex relationships between DCN and A1 bimodal processing in the normal animal provides the basis for studying its disruption in hearing loss and tinnitus models. This article is part of a Special Issue entitled: Tinnitus Neuroscience.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>22995545</pmid><doi>10.1016/j.brainres.2012.08.037</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic Stimulation Animals Auditory Cortex - chemistry Auditory Cortex - physiology Auditory pathways Auditory Perception - physiology Bimodal integration Brain Brain stem Brain Stem - chemistry Brain Stem - physiology Cochlear nuclei Cochlear Nucleus - physiology cortex Cortex (auditory) Cortex (somatosensory) Data Interpretation, Statistical Dorsal cochlear nucleus Electric Stimulation Electrodes Electrophysiological Phenomena Female Firing pattern Firing rate Guinea Pigs hearing Hearing loss Integration Nervous system Neurology Neuronal Plasticity - physiology Neurons - physiology Perception Physical Stimulation Primary auditory cortex Pyramidal cells Sensory integration Somatosensory Somatosensory system Spinal trigeminal nucleus Tinnitus Tinnitus - physiopathology Trigeminal Nuclei - physiology Unit activity |
title | Multi-sensory integration in brainstem and auditory cortex |
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