Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex
Abstract Reward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. Yet, it is unknown, how the VTA infl...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2019-12-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-019-56926-6 |
| _version_ | 1831707821009272832 |
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| author | Michael G. K. Brunk Katrina E. Deane Martin Kisse Matthias Deliano Silvia Vieweg Frank W. Ohl Michael T. Lippert Max F. K. Happel |
| author_facet | Michael G. K. Brunk Katrina E. Deane Martin Kisse Matthias Deliano Silvia Vieweg Frank W. Ohl Michael T. Lippert Max F. K. Happel |
| author_sort | Michael G. K. Brunk |
| collection | DOAJ |
| description | Abstract Reward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. Yet, it is unknown, how the VTA influences cortical frequency processing and spectral integration. Therefore, we investigated the temporal effects of direct optogenetic stimulation of the VTA onto spectral integration in the auditory cortex on a synaptic circuit level by current-source-density analysis in anesthetized Mongolian gerbils. While auditory lemniscal input predominantly terminates in the granular input layers III/IV, we found that VTA-mediated modulation of spectral processing is relayed by a different circuit, namely enhanced thalamic inputs to the infragranular layers Vb/VIa. Activation of this circuit yields a frequency-specific gain amplification of local sensory input and enhances corticocortical information transfer, especially in supragranular layers I/II. This effects persisted over more than 30 minutes after VTA stimulation. Altogether, we demonstrate that the VTA exhibits a long-lasting influence on sensory cortical processing via infragranular layers transcending the signaling of a mere reward-prediction error. We thereby demonstrate a cellular and circuit substrate for the influence of reinforcement-evaluating brain systems on sensory processing in the auditory cortex. |
| first_indexed | 2024-12-20T21:46:37Z |
| format | Article |
| id | doaj.art-2ed2eb32b1524790967f39e9fa60417a |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-20T21:46:37Z |
| publishDate | 2019-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-2ed2eb32b1524790967f39e9fa60417a2022-12-21T19:25:40ZengNature PortfolioScientific Reports2045-23222019-12-019111510.1038/s41598-019-56926-6Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortexMichael G. K. Brunk0Katrina E. Deane1Martin Kisse2Matthias Deliano3Silvia Vieweg4Frank W. Ohl5Michael T. Lippert6Max F. K. Happel7Department of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyDepartment of Systems Physiology of Learning, Leibniz Institute for NeurobiologyAbstract Reward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. Yet, it is unknown, how the VTA influences cortical frequency processing and spectral integration. Therefore, we investigated the temporal effects of direct optogenetic stimulation of the VTA onto spectral integration in the auditory cortex on a synaptic circuit level by current-source-density analysis in anesthetized Mongolian gerbils. While auditory lemniscal input predominantly terminates in the granular input layers III/IV, we found that VTA-mediated modulation of spectral processing is relayed by a different circuit, namely enhanced thalamic inputs to the infragranular layers Vb/VIa. Activation of this circuit yields a frequency-specific gain amplification of local sensory input and enhances corticocortical information transfer, especially in supragranular layers I/II. This effects persisted over more than 30 minutes after VTA stimulation. Altogether, we demonstrate that the VTA exhibits a long-lasting influence on sensory cortical processing via infragranular layers transcending the signaling of a mere reward-prediction error. We thereby demonstrate a cellular and circuit substrate for the influence of reinforcement-evaluating brain systems on sensory processing in the auditory cortex.https://doi.org/10.1038/s41598-019-56926-6 |
| spellingShingle | Michael G. K. Brunk Katrina E. Deane Martin Kisse Matthias Deliano Silvia Vieweg Frank W. Ohl Michael T. Lippert Max F. K. Happel Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex Scientific Reports |
| title | Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| title_full | Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| title_fullStr | Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| title_full_unstemmed | Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| title_short | Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| title_sort | optogenetic stimulation of the vta modulates a frequency specific gain of thalamocortical inputs in infragranular layers of the auditory cortex |
| url | https://doi.org/10.1038/s41598-019-56926-6 |
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