The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making

The inferior colliculus (IC) has traditionally been regarded as an important relay in the auditory pathway, primarily involved in relaying auditory information from the brainstem to the thalamus. However, this study uncovers the multifaceted role of the IC in bridging auditory processing, sensory pr...

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Main Authors: Xinyu Du, Haoxuan Xu, Peirun Song, Yuying Zhai, Hangting Ye, Xuehui Bao, Qianyue Huang, Hisashi Tanigawa, Zhiyi Tu, Pei Chen, Xuan Zhao, Josef P Rauschecker, Xiongjie Yu
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Language:English
Published: eLife Sciences Publications Ltd 2025-01-01
Series:eLife
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Online Access:https://elifesciences.org/articles/101142
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author Xinyu Du
Haoxuan Xu
Peirun Song
Yuying Zhai
Hangting Ye
Xuehui Bao
Qianyue Huang
Hisashi Tanigawa
Zhiyi Tu
Pei Chen
Xuan Zhao
Josef P Rauschecker
Xiongjie Yu
author_facet Xinyu Du
Haoxuan Xu
Peirun Song
Yuying Zhai
Hangting Ye
Xuehui Bao
Qianyue Huang
Hisashi Tanigawa
Zhiyi Tu
Pei Chen
Xuan Zhao
Josef P Rauschecker
Xiongjie Yu
author_sort Xinyu Du
collection DOAJ
description The inferior colliculus (IC) has traditionally been regarded as an important relay in the auditory pathway, primarily involved in relaying auditory information from the brainstem to the thalamus. However, this study uncovers the multifaceted role of the IC in bridging auditory processing, sensory prediction, and reward prediction. Through extracellular recordings in monkeys engaged in a sound duration-based deviation detection task, we observed a 'climbing effect' in neuronal firing rates, indicative of an enhanced response over sound sequences linked to sensory prediction rather than reward anticipation. Moreover, our findings demonstrate reward prediction errors within the IC, highlighting its complex integration in auditory and reward processing. Further analysis revealed a direct correlation between IC neuronal activity and behavioral choices, suggesting its involvement in decision-making processes. This research highlights a more complex role for the IC than traditionally understood, showcasing its integral role in cognitive and sensory processing and emphasizing its importance in integrated brain functions.
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publisher eLife Sciences Publications Ltd
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series eLife
spelling doaj-art-eee677ac2b1d4b76a40cbcb47a37904d2025-01-29T18:01:18ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.101142The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-makingXinyu Du0https://orcid.org/0009-0001-7773-1835Haoxuan Xu1https://orcid.org/0000-0002-7316-8440Peirun Song2Yuying Zhai3Hangting Ye4Xuehui Bao5Qianyue Huang6Hisashi Tanigawa7https://orcid.org/0000-0002-7736-0683Zhiyi Tu8Pei Chen9Xuan Zhao10Josef P Rauschecker11Xiongjie Yu12https://orcid.org/0000-0002-0040-2187Department of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaCollege of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China; Key Laboratory for Biomedical Engineering of Ministry of Education, Hangzhou, ChinaDepartment of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaDepartment of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, ChinaCollege of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China; Key Laboratory for Biomedical Engineering of Ministry of Education, Hangzhou, ChinaCollege of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China; Key Laboratory for Biomedical Engineering of Ministry of Education, Hangzhou, ChinaCollege of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China; Key Laboratory for Biomedical Engineering of Ministry of Education, Hangzhou, ChinaDepartment of Anesthesiology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, ChinaDepartment of Anesthesiology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, ChinaDepartment of Anesthesiology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, ChinaDepartment of Neuroscience, Georgetown University, Washington, DC, United StatesDepartment of Anesthesia, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; Zhejiang Provincial Key Laboratory of Precision Diagnosis and Therapy for Major Gynecological Diseases, Women's Hospital, Zhejiang University School of Medicine, Hangzhou, China; College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China; Key Laboratory for Biomedical Engineering of Ministry of Education, Hangzhou, China; Department of Anesthesiology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, ChinaThe inferior colliculus (IC) has traditionally been regarded as an important relay in the auditory pathway, primarily involved in relaying auditory information from the brainstem to the thalamus. However, this study uncovers the multifaceted role of the IC in bridging auditory processing, sensory prediction, and reward prediction. Through extracellular recordings in monkeys engaged in a sound duration-based deviation detection task, we observed a 'climbing effect' in neuronal firing rates, indicative of an enhanced response over sound sequences linked to sensory prediction rather than reward anticipation. Moreover, our findings demonstrate reward prediction errors within the IC, highlighting its complex integration in auditory and reward processing. Further analysis revealed a direct correlation between IC neuronal activity and behavioral choices, suggesting its involvement in decision-making processes. This research highlights a more complex role for the IC than traditionally understood, showcasing its integral role in cognitive and sensory processing and emphasizing its importance in integrated brain functions.https://elifesciences.org/articles/101142inferior colliculussound durationdecision makingprediction errorreward behavior
spellingShingle Xinyu Du
Haoxuan Xu
Peirun Song
Yuying Zhai
Hangting Ye
Xuehui Bao
Qianyue Huang
Hisashi Tanigawa
Zhiyi Tu
Pei Chen
Xuan Zhao
Josef P Rauschecker
Xiongjie Yu
The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
eLife
inferior colliculus
sound duration
decision making
prediction error
reward behavior
title The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
title_full The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
title_fullStr The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
title_full_unstemmed The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
title_short The multifaceted role of the inferior colliculus in sensory prediction, reward processing, and decision-making
title_sort multifaceted role of the inferior colliculus in sensory prediction reward processing and decision making
topic inferior colliculus
sound duration
decision making
prediction error
reward behavior
url https://elifesciences.org/articles/101142
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