Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini, Ingrid Bethus
{"title":"学习过程中纹状体网络的编码动态","authors":"Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini, Ingrid Bethus","doi":"10.1523/ENEURO.0436-23.2024","DOIUrl":null,"url":null,"abstract":"<p><p>The rat dorsomedial (DMS) and dorsolateral striatum (DLS), equivalent to caudate nucleus and putamen in primates, are required for goal-directed and habit behaviour, respectively. However, it is still unclear whether and how this functional dichotomy emerges in the course of learning. In this study, we investigated this issue by recording DMS and DLS single neuron activity in rats performing a continuous spatial alternation task, from the acquisition to optimized performance. We first applied a classical analytical approach to identify task-related activity based on the modifications of single neuron firing rate in relation to specific task events or maze trajectories. We then used an innovative approach based on Hawkes process to reconstruct a directed connectivity graph of simultaneously recorded neurons, that was used to decode animal behavior. This approach enabled us to better unravel the role of DMS and DLS neural networks across learning stages. We showed that DMS and DLS display different task-related activity throughout learning stages, and the proportion of coding neurons over time decreases in the DMS and increases in the DLS. Despite these major differences, the decoding power of both networks increases during learning. These results suggest that DMS and DLS neural networks gradually reorganize in different ways in order to progressively increase their control over the behavioral performance.</p>","PeriodicalId":11617,"journal":{"name":"eNeuro","volume":" ","pages":""},"PeriodicalIF":2.7000,"publicationDate":"2024-10-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521795/pdf/","citationCount":"0","resultStr":"{\"title\":\"Coding Dynamics of the Striatal Networks During Learning.\",\"authors\":\"Maxime Villet, Patricia Reynaud-Bouret, Julien Poitreau, Jacopo Baldi, Sophie Jaffard, Ashwin James, Alexandre Muzy, Evgenia Kartsaki, Gilles Scarella, Francesca Sargolini, Ingrid Bethus\",\"doi\":\"10.1523/ENEURO.0436-23.2024\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The rat dorsomedial (DMS) and dorsolateral striatum (DLS), equivalent to caudate nucleus and putamen in primates, are required for goal-directed and habit behaviour, respectively. However, it is still unclear whether and how this functional dichotomy emerges in the course of learning. In this study, we investigated this issue by recording DMS and DLS single neuron activity in rats performing a continuous spatial alternation task, from the acquisition to optimized performance. We first applied a classical analytical approach to identify task-related activity based on the modifications of single neuron firing rate in relation to specific task events or maze trajectories. We then used an innovative approach based on Hawkes process to reconstruct a directed connectivity graph of simultaneously recorded neurons, that was used to decode animal behavior. This approach enabled us to better unravel the role of DMS and DLS neural networks across learning stages. We showed that DMS and DLS display different task-related activity throughout learning stages, and the proportion of coding neurons over time decreases in the DMS and increases in the DLS. Despite these major differences, the decoding power of both networks increases during learning. These results suggest that DMS and DLS neural networks gradually reorganize in different ways in order to progressively increase their control over the behavioral performance.</p>\",\"PeriodicalId\":11617,\"journal\":{\"name\":\"eNeuro\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":2.7000,\"publicationDate\":\"2024-10-29\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521795/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"eNeuro\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1523/ENEURO.0436-23.2024\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/10/1 0:00:00\",\"PubModel\":\"Print\",\"JCR\":\"Q3\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"eNeuro","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/ENEURO.0436-23.2024","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/1 0:00:00","PubModel":"Print","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Coding Dynamics of the Striatal Networks During Learning.
The rat dorsomedial (DMS) and dorsolateral striatum (DLS), equivalent to caudate nucleus and putamen in primates, are required for goal-directed and habit behaviour, respectively. However, it is still unclear whether and how this functional dichotomy emerges in the course of learning. In this study, we investigated this issue by recording DMS and DLS single neuron activity in rats performing a continuous spatial alternation task, from the acquisition to optimized performance. We first applied a classical analytical approach to identify task-related activity based on the modifications of single neuron firing rate in relation to specific task events or maze trajectories. We then used an innovative approach based on Hawkes process to reconstruct a directed connectivity graph of simultaneously recorded neurons, that was used to decode animal behavior. This approach enabled us to better unravel the role of DMS and DLS neural networks across learning stages. We showed that DMS and DLS display different task-related activity throughout learning stages, and the proportion of coding neurons over time decreases in the DMS and increases in the DLS. Despite these major differences, the decoding power of both networks increases during learning. These results suggest that DMS and DLS neural networks gradually reorganize in different ways in order to progressively increase their control over the behavioral performance.
期刊介绍:
An open-access journal from the Society for Neuroscience, eNeuro publishes high-quality, broad-based, peer-reviewed research focused solely on the field of neuroscience. eNeuro embodies an emerging scientific vision that offers a new experience for authors and readers, all in support of the Society’s mission to advance understanding of the brain and nervous system.