Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning
Summary: In current models, learning the relationship between environmental stimuli and the outcomes of actions involves both stimulus-driven and goal-directed systems, mediated in part by the DLS and DMS, respectively. However, though these models emphasize the importance of the DLS in governing ac...
Main Authors: | , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2018-05-01
|
Series: | Cell Reports |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124718306405 |
_version_ | 1811277014976430080 |
---|---|
author | Hadley C. Bergstrom Anna M. Lipkin Abby G. Lieberman Courtney R. Pinard Ozge Gunduz-Cinar Emma T. Brockway William W. Taylor Mio Nonaka Olena Bukalo Tiffany A. Wills F. Javier Rubio Xuan Li Charles L. Pickens Danny G. Winder Andrew Holmes |
author_facet | Hadley C. Bergstrom Anna M. Lipkin Abby G. Lieberman Courtney R. Pinard Ozge Gunduz-Cinar Emma T. Brockway William W. Taylor Mio Nonaka Olena Bukalo Tiffany A. Wills F. Javier Rubio Xuan Li Charles L. Pickens Danny G. Winder Andrew Holmes |
author_sort | Hadley C. Bergstrom |
collection | DOAJ |
description | Summary: In current models, learning the relationship between environmental stimuli and the outcomes of actions involves both stimulus-driven and goal-directed systems, mediated in part by the DLS and DMS, respectively. However, though these models emphasize the importance of the DLS in governing actions after extensive experience has accumulated, there is growing evidence of DLS engagement from the onset of training. Here, we used in vivo photosilencing to reveal that DLS recruitment interferes with early touchscreen discrimination learning. We also show that the direct output pathway of the DLS is preferentially recruited and causally involved in early learning and find that silencing the normal contribution of the DLS produces plasticity-related alterations in a PL-DMS circuit. These data provide further evidence suggesting that the DLS is recruited in the construction of stimulus-elicited actions that ultimately automate behavior and liberate cognitive resources for other demands, but with a cost to performance at the outset of learning. : What is the contribution of the DLS in early discrimination learning? Bergstrom et al. show using in vivo optogenetics, fluorescence in situ hybridization, and brain-wide activity mapping that silencing the DLS facilitates early discrimination learning, drives activity in a parallel PL-DMS circuit, and preferentially recruits the DLS “direct” output pathway. Keywords: striatum, reward, goal-directed, habit, optogenetics, plasticity, cognition, Arc |
first_indexed | 2024-04-13T00:08:03Z |
format | Article |
id | doaj.art-6f6062c58ca447a3b0ade66fe7c878e4 |
institution | Directory Open Access Journal |
issn | 2211-1247 |
language | English |
last_indexed | 2024-04-13T00:08:03Z |
publishDate | 2018-05-01 |
publisher | Elsevier |
record_format | Article |
series | Cell Reports |
spelling | doaj.art-6f6062c58ca447a3b0ade66fe7c878e42022-12-22T03:11:11ZengElsevierCell Reports2211-12472018-05-0123822642272Dorsolateral Striatum Engagement Interferes with Early Discrimination LearningHadley C. Bergstrom0Anna M. Lipkin1Abby G. Lieberman2Courtney R. Pinard3Ozge Gunduz-Cinar4Emma T. Brockway5William W. Taylor6Mio Nonaka7Olena Bukalo8Tiffany A. Wills9F. Javier Rubio10Xuan Li11Charles L. Pickens12Danny G. Winder13Andrew Holmes14Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA; Corresponding authorLaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USADepartment of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USABehavioral Neuroscience Research Branch, National Institute on Drug Abuse, NIH, Baltimore, MD, USABehavioral Neuroscience Research Branch, National Institute on Drug Abuse, NIH, Baltimore, MD, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USADepartment of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USA; Vanderbilt Center for Addiction Research, Nashville, TN, USALaboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USASummary: In current models, learning the relationship between environmental stimuli and the outcomes of actions involves both stimulus-driven and goal-directed systems, mediated in part by the DLS and DMS, respectively. However, though these models emphasize the importance of the DLS in governing actions after extensive experience has accumulated, there is growing evidence of DLS engagement from the onset of training. Here, we used in vivo photosilencing to reveal that DLS recruitment interferes with early touchscreen discrimination learning. We also show that the direct output pathway of the DLS is preferentially recruited and causally involved in early learning and find that silencing the normal contribution of the DLS produces plasticity-related alterations in a PL-DMS circuit. These data provide further evidence suggesting that the DLS is recruited in the construction of stimulus-elicited actions that ultimately automate behavior and liberate cognitive resources for other demands, but with a cost to performance at the outset of learning. : What is the contribution of the DLS in early discrimination learning? Bergstrom et al. show using in vivo optogenetics, fluorescence in situ hybridization, and brain-wide activity mapping that silencing the DLS facilitates early discrimination learning, drives activity in a parallel PL-DMS circuit, and preferentially recruits the DLS “direct” output pathway. Keywords: striatum, reward, goal-directed, habit, optogenetics, plasticity, cognition, Archttp://www.sciencedirect.com/science/article/pii/S2211124718306405 |
spellingShingle | Hadley C. Bergstrom Anna M. Lipkin Abby G. Lieberman Courtney R. Pinard Ozge Gunduz-Cinar Emma T. Brockway William W. Taylor Mio Nonaka Olena Bukalo Tiffany A. Wills F. Javier Rubio Xuan Li Charles L. Pickens Danny G. Winder Andrew Holmes Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning Cell Reports |
title | Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning |
title_full | Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning |
title_fullStr | Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning |
title_full_unstemmed | Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning |
title_short | Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning |
title_sort | dorsolateral striatum engagement interferes with early discrimination learning |
url | http://www.sciencedirect.com/science/article/pii/S2211124718306405 |
work_keys_str_mv | AT hadleycbergstrom dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT annamlipkin dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT abbyglieberman dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT courtneyrpinard dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT ozgegunduzcinar dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT emmatbrockway dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT williamwtaylor dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT miononaka dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT olenabukalo dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT tiffanyawills dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT fjavierrubio dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT xuanli dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT charleslpickens dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT dannygwinder dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning AT andrewholmes dorsolateralstriatumengagementinterfereswithearlydiscriminationlearning |