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...

Full description

Bibliographic Details
Main Authors: 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
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