Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum
The striatum, the central hub of cortico-basal ganglia loops, contains functionally heterogeneous subregions distinguished by the topographic patterns of structural connectivity. These subregions mediate various processes of procedural learning. However, it remains unclear when and how striatal subr...
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| Format: | Article |
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eLife Sciences Publications Ltd
2025-07-01
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| Online Access: | https://elifesciences.org/articles/97326 |
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| author | Susumu Setogawa Takashi Okauchi Di Hu Yasuhiro Wada Keigo Hikishima Hirotaka Onoe Kayo Nishizawa Nobuyuki Sakayori Hiroyuki Miyawaki Takuma Kitanishi Kenji Mizuseki Yilong Cui Kazuto Kobayashi |
| author_facet | Susumu Setogawa Takashi Okauchi Di Hu Yasuhiro Wada Keigo Hikishima Hirotaka Onoe Kayo Nishizawa Nobuyuki Sakayori Hiroyuki Miyawaki Takuma Kitanishi Kenji Mizuseki Yilong Cui Kazuto Kobayashi |
| author_sort | Susumu Setogawa |
| collection | DOAJ |
| description | The striatum, the central hub of cortico-basal ganglia loops, contains functionally heterogeneous subregions distinguished by the topographic patterns of structural connectivity. These subregions mediate various processes of procedural learning. However, it remains unclear when and how striatal subregions engage in the acquisition of sensory stimulus-based decision-making. A neuroimaging of regional brain activity shows that the anterior dorsolateral striatum (aDLS) and posterior ventrolateral striatum (pVLS) in rats are activated in a different temporal pattern during the acquisition phase of auditory discrimination. Chronic and transient pharmacologic manipulations show that the aDLS promotes the behavioral strategy driven by the stimulus-response association while suppressing that by the response-outcome association, and that the pVLS contributes to forming and maintaining the stimulus-response strategy. Electrophysiological recording indicates that subpopulations of aDLS neurons predominantly represent the outcome of specific behaviors at the initial period of discrimination learning, and that pVLS subpopulations encode the beginning and ending of each behavior according to the progress of learning. In addition, other subpopulations of striatal neurons indicate sustained activation after obtaining reward with distinct patterns reflecting the stimulus-response associations. Our findings demonstrate that aDLS and pVLS neurons integrate the new learning of auditory discrimination in spatiotemporally and functionally different manners. |
| format | Article |
| id | doaj-art-82d7bcba837741ae9dafd30cac71e7ec |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-82d7bcba837741ae9dafd30cac71e7ec2025-08-20T03:28:26ZengeLife Sciences Publications LtdeLife2050-084X2025-07-011310.7554/eLife.97326Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatumSusumu Setogawa0https://orcid.org/0000-0002-9161-2656Takashi Okauchi1Di Hu2Yasuhiro Wada3Keigo Hikishima4Hirotaka Onoe5Kayo Nishizawa6Nobuyuki Sakayori7Hiroyuki Miyawaki8Takuma Kitanishi9Kenji Mizuseki10https://orcid.org/0000-0002-1456-2149Yilong Cui11Kazuto Kobayashi12https://orcid.org/0000-0002-7617-2939Department of Physiology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan; Department of Physiology, Osaka City University Graduate School of Medicine, Osaka, Japan; Department of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University, Fukushima, Japan; Laboratory for Biofunction Dynamics Imaging, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan; Japan Society for the Promotion of Science, Tokyo, JapanLaboratory for Biofunction Dynamics Imaging, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanLaboratory for Biofunction Dynamics Imaging, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanLaboratory for Pathophysiological and Health Science, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanMedical Devices Research Group, Health and Medical Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, JapanHuman Brain Research Center, Kyoto University Graduate School of Medicine, Kyoto, JapanDepartment of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University, Fukushima, JapanDepartment of Physiology and Oral Physiology, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima, JapanDepartment of Physiology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan; Department of Physiology, Osaka City University Graduate School of Medicine, Osaka, JapanDepartment of Physiology, Osaka City University Graduate School of Medicine, Osaka, JapanDepartment of Physiology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan; Department of Physiology, Osaka City University Graduate School of Medicine, Osaka, JapanLaboratory for Biofunction Dynamics Imaging, RIKEN Center for Biosystems Dynamics Research, Kobe, JapanDepartment of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University, Fukushima, JapanThe striatum, the central hub of cortico-basal ganglia loops, contains functionally heterogeneous subregions distinguished by the topographic patterns of structural connectivity. These subregions mediate various processes of procedural learning. However, it remains unclear when and how striatal subregions engage in the acquisition of sensory stimulus-based decision-making. A neuroimaging of regional brain activity shows that the anterior dorsolateral striatum (aDLS) and posterior ventrolateral striatum (pVLS) in rats are activated in a different temporal pattern during the acquisition phase of auditory discrimination. Chronic and transient pharmacologic manipulations show that the aDLS promotes the behavioral strategy driven by the stimulus-response association while suppressing that by the response-outcome association, and that the pVLS contributes to forming and maintaining the stimulus-response strategy. Electrophysiological recording indicates that subpopulations of aDLS neurons predominantly represent the outcome of specific behaviors at the initial period of discrimination learning, and that pVLS subpopulations encode the beginning and ending of each behavior according to the progress of learning. In addition, other subpopulations of striatal neurons indicate sustained activation after obtaining reward with distinct patterns reflecting the stimulus-response associations. Our findings demonstrate that aDLS and pVLS neurons integrate the new learning of auditory discrimination in spatiotemporally and functionally different manners.https://elifesciences.org/articles/97326decision makingauditory discriminationstimulus-response associationresponse–outcome associationstriatumevent-related neuron |
| spellingShingle | Susumu Setogawa Takashi Okauchi Di Hu Yasuhiro Wada Keigo Hikishima Hirotaka Onoe Kayo Nishizawa Nobuyuki Sakayori Hiroyuki Miyawaki Takuma Kitanishi Kenji Mizuseki Yilong Cui Kazuto Kobayashi Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum eLife decision making auditory discrimination stimulus-response association response–outcome association striatum event-related neuron |
| title | Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| title_full | Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| title_fullStr | Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| title_full_unstemmed | Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| title_short | Acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| title_sort | acquisition of auditory discrimination mediated by different processes through two distinct circuits linked to the lateral striatum |
| topic | decision making auditory discrimination stimulus-response association response–outcome association striatum event-related neuron |
| url | https://elifesciences.org/articles/97326 |
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