Functional segregation and dynamic integration of the corticotectal descending signal in rat

The superior colliculus (SC) receives inputs from various brain regions in a layer- and radial subregion-specific manner, but whether the SC exhibits subregion-specific dynamics remains unclear. To address this issue, we recorded the spiking activity of single SC neurons while photoactivating cortic...

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Main Authors: Hikaru Sugino, Sho Tanno, Tatsumi Yoshida, Yoshikazu Isomura, Riichiro Hira
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Neuroscience Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S0168010224001111
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author Hikaru Sugino
Sho Tanno
Tatsumi Yoshida
Yoshikazu Isomura
Riichiro Hira
author_facet Hikaru Sugino
Sho Tanno
Tatsumi Yoshida
Yoshikazu Isomura
Riichiro Hira
author_sort Hikaru Sugino
collection DOAJ
description The superior colliculus (SC) receives inputs from various brain regions in a layer- and radial subregion-specific manner, but whether the SC exhibits subregion-specific dynamics remains unclear. To address this issue, we recorded the spiking activity of single SC neurons while photoactivating cortical areas in awake head-fixed Thy1-ChR2 rats. We classified 309 neurons that responded significantly into 8 clusters according to the response dynamics. Among them, neurons with monophasic excitatory responses (7–12 ms latency) that returned to baseline within 20 ms were commonly observed in the optic and intermediate gray layers of centromedial and centrolateral SC. In contrast, neurons with complex polyphasic responses were commonly observed in the deep layers of the anterolateral SC. Cross-correlation analysis suggested that the complex pattern could be only partly explained by an internal circuit of the deep gray layer. Our results indicate that medial to centrolateral SC neurons simply relay cortical activity, whereas neurons in the deep layers of the anterolateral SC dynamically integrate inputs from the cortex, SNr, CN, and local circuits. These findings suggest a spatial gradient in SC integration, with a division of labor between simple relay circuits and those integrating complex dynamics.
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spelling doaj-art-cd10de40c02b44c385bb58c8c74b8bc72025-01-16T04:28:17ZengElsevierNeuroscience Research0168-01022025-01-012103850Functional segregation and dynamic integration of the corticotectal descending signal in ratHikaru Sugino0Sho Tanno1Tatsumi Yoshida2Yoshikazu Isomura3Riichiro Hira4Department of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanDepartment of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanDepartment of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanCorrespondence to: Department of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japan.; Department of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanCorrespondence to: Department of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japan.; Department of Physiology and Cell Biology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, JapanThe superior colliculus (SC) receives inputs from various brain regions in a layer- and radial subregion-specific manner, but whether the SC exhibits subregion-specific dynamics remains unclear. To address this issue, we recorded the spiking activity of single SC neurons while photoactivating cortical areas in awake head-fixed Thy1-ChR2 rats. We classified 309 neurons that responded significantly into 8 clusters according to the response dynamics. Among them, neurons with monophasic excitatory responses (7–12 ms latency) that returned to baseline within 20 ms were commonly observed in the optic and intermediate gray layers of centromedial and centrolateral SC. In contrast, neurons with complex polyphasic responses were commonly observed in the deep layers of the anterolateral SC. Cross-correlation analysis suggested that the complex pattern could be only partly explained by an internal circuit of the deep gray layer. Our results indicate that medial to centrolateral SC neurons simply relay cortical activity, whereas neurons in the deep layers of the anterolateral SC dynamically integrate inputs from the cortex, SNr, CN, and local circuits. These findings suggest a spatial gradient in SC integration, with a division of labor between simple relay circuits and those integrating complex dynamics.http://www.sciencedirect.com/science/article/pii/S0168010224001111Superior colliculusCerebral cortexElectrophysiologyDynamicsOptogeneticsNeuropixels
spellingShingle Hikaru Sugino
Sho Tanno
Tatsumi Yoshida
Yoshikazu Isomura
Riichiro Hira
Functional segregation and dynamic integration of the corticotectal descending signal in rat
Neuroscience Research
Superior colliculus
Cerebral cortex
Electrophysiology
Dynamics
Optogenetics
Neuropixels
title Functional segregation and dynamic integration of the corticotectal descending signal in rat
title_full Functional segregation and dynamic integration of the corticotectal descending signal in rat
title_fullStr Functional segregation and dynamic integration of the corticotectal descending signal in rat
title_full_unstemmed Functional segregation and dynamic integration of the corticotectal descending signal in rat
title_short Functional segregation and dynamic integration of the corticotectal descending signal in rat
title_sort functional segregation and dynamic integration of the corticotectal descending signal in rat
topic Superior colliculus
Cerebral cortex
Electrophysiology
Dynamics
Optogenetics
Neuropixels
url http://www.sciencedirect.com/science/article/pii/S0168010224001111
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