Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning
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
Affiliations
Hadley C. Bergstrom
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA; Corresponding author
Anna M. Lipkin
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Abby G. Lieberman
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Courtney R. Pinard
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Ozge Gunduz-Cinar
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Emma T. Brockway
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
William W. Taylor
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Mio Nonaka
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Olena Bukalo
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Tiffany A. Wills
Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USA
F. Javier Rubio
Behavioral Neuroscience Research Branch, National Institute on Drug Abuse, NIH, Baltimore, MD, USA
Xuan Li
Behavioral Neuroscience Research Branch, National Institute on Drug Abuse, NIH, Baltimore, MD, USA
Charles L. Pickens
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
Danny G. Winder
Department of Molecular Physiology and Biophysics, Vanderbilt University, Nashville, TN, USA; Vanderbilt Center for Addiction Research, Nashville, TN, USA
Andrew Holmes
Laboratory of Behavioral and Genomic Neuroscience, National Institute on Alcohol Abuse and Alcoholism, NIH, Bethesda, MD, USA
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
