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...
Saved in:
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2025-01-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/101142 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1832582484273922048 |
---|---|
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. |
format | Article |
id | doaj-art-eee677ac2b1d4b76a40cbcb47a37904d |
institution | Kabale University |
issn | 2050-084X |
language | English |
publishDate | 2025-01-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
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 |
work_keys_str_mv | AT xinyudu themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT haoxuanxu themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT peirunsong themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT yuyingzhai themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT hangtingye themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xuehuibao themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT qianyuehuang themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT hisashitanigawa themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT zhiyitu themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT peichen themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xuanzhao themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT josefprauschecker themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xiongjieyu themultifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xinyudu multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT haoxuanxu multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT peirunsong multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT yuyingzhai multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT hangtingye multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xuehuibao multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT qianyuehuang multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT hisashitanigawa multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT zhiyitu multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT peichen multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xuanzhao multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT josefprauschecker multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking AT xiongjieyu multifacetedroleoftheinferiorcolliculusinsensorypredictionrewardprocessinganddecisionmaking |