Lena S Geiger, Torsten Wüstenberg, Zhenxiang Zang, Mirjam Melzer, Stephanie H Witt, Marcella Rietschel, Markus M Nöthen, Stefan Herms, Franziska Degenhardt, Andreas Meyer-Lindenberg, Carolin Moessnang
{"title":"前额纹状体回路中认知程序学习的纵向标记以及 BDNF 可塑性相关变体的推定效应。","authors":"Lena S Geiger, Torsten Wüstenberg, Zhenxiang Zang, Mirjam Melzer, Stephanie H Witt, Marcella Rietschel, Markus M Nöthen, Stefan Herms, Franziska Degenhardt, Andreas Meyer-Lindenberg, Carolin Moessnang","doi":"10.1038/s41539-024-00282-2","DOIUrl":null,"url":null,"abstract":"<p><p>Procedural learning and automatization have widely been studied in behavioral psychology and typically involves a rapid improvement, followed by a plateau in performance throughout repeated training. More recently, brain imaging studies have implicated frontal-striatal brain circuits in skill learning. However, it is largely unknown whether frontal-striatal activation during skill learning and behavioral changes follow a similar learning curve pattern. To address this gap in knowledge, we performed a longitudinal brain imaging study using a procedural working memory (pWM) task with repeated measurements across two weeks to map the temporal dynamics of skill learning. We additionally explored the effect of the BDNF Val<sup>66</sup>Met polymorphism, a common genetic polymorphism impacting neural plasticity, to further inform the relevance of the identified neural markers. We used linear and exponential modeling to characterize procedural learning by means of learning curves on the behavioral and brain functional level. We show that repeated training led to an exponential decay in a distributed set of brain regions including fronto-striatal circuits, which paralleled the exponential improvement in task performance. In addition, we show that both behavioral and neurofunctional readouts were sensitive to the BDNF Val<sup>66</sup>Met polymorphism, suggesting less efficient learning in <sup>66</sup>Met-allele carriers along with protracted signal decay in frontal and striatal brain regions. Our results extend existing literature by showing the temporal relationship between procedural learning and frontal-striatal brain function and suggest a role of BDNF in mediating neural plasticity for establishing automatized behavior.</p>","PeriodicalId":48503,"journal":{"name":"npj Science of Learning","volume":"9 1","pages":"72"},"PeriodicalIF":3.6000,"publicationDate":"2024-11-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11603174/pdf/","citationCount":"0","resultStr":"{\"title\":\"Longitudinal markers of cognitive procedural learning in fronto-striatal circuits and putative effects of a BDNF plasticity-related variant.\",\"authors\":\"Lena S Geiger, Torsten Wüstenberg, Zhenxiang Zang, Mirjam Melzer, Stephanie H Witt, Marcella Rietschel, Markus M Nöthen, Stefan Herms, Franziska Degenhardt, Andreas Meyer-Lindenberg, Carolin Moessnang\",\"doi\":\"10.1038/s41539-024-00282-2\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Procedural learning and automatization have widely been studied in behavioral psychology and typically involves a rapid improvement, followed by a plateau in performance throughout repeated training. More recently, brain imaging studies have implicated frontal-striatal brain circuits in skill learning. However, it is largely unknown whether frontal-striatal activation during skill learning and behavioral changes follow a similar learning curve pattern. To address this gap in knowledge, we performed a longitudinal brain imaging study using a procedural working memory (pWM) task with repeated measurements across two weeks to map the temporal dynamics of skill learning. We additionally explored the effect of the BDNF Val<sup>66</sup>Met polymorphism, a common genetic polymorphism impacting neural plasticity, to further inform the relevance of the identified neural markers. We used linear and exponential modeling to characterize procedural learning by means of learning curves on the behavioral and brain functional level. We show that repeated training led to an exponential decay in a distributed set of brain regions including fronto-striatal circuits, which paralleled the exponential improvement in task performance. In addition, we show that both behavioral and neurofunctional readouts were sensitive to the BDNF Val<sup>66</sup>Met polymorphism, suggesting less efficient learning in <sup>66</sup>Met-allele carriers along with protracted signal decay in frontal and striatal brain regions. Our results extend existing literature by showing the temporal relationship between procedural learning and frontal-striatal brain function and suggest a role of BDNF in mediating neural plasticity for establishing automatized behavior.</p>\",\"PeriodicalId\":48503,\"journal\":{\"name\":\"npj Science of Learning\",\"volume\":\"9 1\",\"pages\":\"72\"},\"PeriodicalIF\":3.6000,\"publicationDate\":\"2024-11-28\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11603174/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"npj Science of Learning\",\"FirstCategoryId\":\"102\",\"ListUrlMain\":\"https://doi.org/10.1038/s41539-024-00282-2\",\"RegionNum\":1,\"RegionCategory\":\"心理学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"EDUCATION & EDUCATIONAL RESEARCH\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"npj Science of Learning","FirstCategoryId":"102","ListUrlMain":"https://doi.org/10.1038/s41539-024-00282-2","RegionNum":1,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"EDUCATION & EDUCATIONAL RESEARCH","Score":null,"Total":0}
Longitudinal markers of cognitive procedural learning in fronto-striatal circuits and putative effects of a BDNF plasticity-related variant.
Procedural learning and automatization have widely been studied in behavioral psychology and typically involves a rapid improvement, followed by a plateau in performance throughout repeated training. More recently, brain imaging studies have implicated frontal-striatal brain circuits in skill learning. However, it is largely unknown whether frontal-striatal activation during skill learning and behavioral changes follow a similar learning curve pattern. To address this gap in knowledge, we performed a longitudinal brain imaging study using a procedural working memory (pWM) task with repeated measurements across two weeks to map the temporal dynamics of skill learning. We additionally explored the effect of the BDNF Val66Met polymorphism, a common genetic polymorphism impacting neural plasticity, to further inform the relevance of the identified neural markers. We used linear and exponential modeling to characterize procedural learning by means of learning curves on the behavioral and brain functional level. We show that repeated training led to an exponential decay in a distributed set of brain regions including fronto-striatal circuits, which paralleled the exponential improvement in task performance. In addition, we show that both behavioral and neurofunctional readouts were sensitive to the BDNF Val66Met polymorphism, suggesting less efficient learning in 66Met-allele carriers along with protracted signal decay in frontal and striatal brain regions. Our results extend existing literature by showing the temporal relationship between procedural learning and frontal-striatal brain function and suggest a role of BDNF in mediating neural plasticity for establishing automatized behavior.