Episodic Memory Encoding Interferes with Reward Learning and Decreases Striatal Prediction Errors

被引:86
|
作者
Wimmer, G. Elliott [1 ,3 ]
Braun, Erin Kendall [1 ]
Daw, Nathaniel D. [4 ,5 ]
Shohamy, Daphna [1 ,2 ]
机构
[1] Columbia Univ, Dept Psychol, New York, NY 10027 USA
[2] Columbia Univ, Kavli Inst Brain Sci, New York, NY 10027 USA
[3] Univ Med Ctr Hamburg Eppendorf, Dept Syst Neurosci, D-20246 Hamburg, Germany
[4] NYU, Ctr Neural Sci, New York, NY 10003 USA
[5] NYU, Dept Psychol, New York, NY 10003 USA
来源
JOURNAL OF NEUROSCIENCE | 2014年 / 34卷 / 45期
基金
美国国家科学基金会;
关键词
decision making; hippocampus; learning; memory; reward; striatum; BRAIN ACTIVITY; HIPPOCAMPUS; MODEL; SIGNALS; SYSTEMS; FMRI; REPRESENTATION; VISUALIZATION; NEUROBIOLOGY; INFORMATION;
D O I
10.1523/JNEUROSCI.0204-14.2014
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Learning is essential for adaptive decision making. The striatum and its dopaminergic inputs are known to support incremental reward-based learning, while the hippocampus is known to support encoding of single events (episodic memory). Although traditionally studied separately, in even simple experiences, these two types of learning are likely to co-occur and may interact. Here we sought to understand the nature of this interaction by examining how incremental reward learning is related to concurrent episodic memory encoding. During the experiment, human participants made choices between two options (colored squares), each associated with a drifting probability of reward, with the goal of earning as much money as possible. Incidental, trial-unique object pictures, unrelated to the choice, were overlaid on each option. The next day, participants were given a surprise memory test for these pictures. We found that better episodic memory was related to a decreased influence of recent reward experience on choice, both within and across participants. fMRI analyses further revealed that during learning the canonical striatal reward prediction error signal was significantly weaker when episodic memory was stronger. This decrease in reward prediction error signals in the striatum was associated with enhanced functional connectivity between the hippocampus and striatum at the time of choice. Our results suggest a mechanism by which memory encoding may compete for striatal processing and provide insight into how interactions between different forms of learning guide reward-based decision making.
引用
收藏
页码:14901 / 14912
页数:12
相关论文
共 50 条
  • [41] Dopamine transients encode reward prediction errors independent of learning rates
    Mah, Andrew
    Golden, Carla E. M.
    Constantinople, Christine M.
    CELL REPORTS, 2024, 43 (10):
  • [42] Musical reward prediction errors engage the nucleus accumbens and motivate learning
    Gold, Benjamin P.
    Mas-Herrero, Ernest
    Zeighami, Yashar
    Benovoy, Mitchel
    Dagher, Alain
    Zatorre, Robert J.
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2019, 116 (08) : 3310 - 3315
  • [43] Human neural learning depends on reward prediction errors in the blocking paradigm
    Tobler, PN
    O'Doherty, JP
    Dolan, RJ
    Schultz, W
    JOURNAL OF NEUROPHYSIOLOGY, 2006, 95 (01) : 301 - 310
  • [44] Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
    Oettl, Lars-Lennart
    Scheller, Max
    Filosa, Carla
    Wieland, Sebastian
    Haag, Franziska
    Loeb, Cathrin
    Durstewitz, Daniel
    Shusterman, Roman
    Russo, Eleonora
    Kelsch, Wolfgang
    NATURE COMMUNICATIONS, 2020, 11 (01)
  • [45] Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
    Lars-Lennart Oettl
    Max Scheller
    Carla Filosa
    Sebastian Wieland
    Franziska Haag
    Cathrin Loeb
    Daniel Durstewitz
    Roman Shusterman
    Eleonora Russo
    Wolfgang Kelsch
    Nature Communications, 11
  • [46] The contribution of striatal pseudo-reward prediction errors to value-based decision-making
    Mas-Herrero, Ernest
    Sescousse, Guillaume
    Cools, Roshan
    Marco-Pallares, Josep
    NEUROIMAGE, 2019, 193 : 67 - 74
  • [47] Effects of Opioid Use Disorder and Withdrawal on Striatal Reward Prediction Errors During Decision-Making
    Wesley, Michael
    Beckmann, Joshua
    Babalonis, Shanna
    Alcorn, Joseph
    Hatton, Kevin
    Lon, Hays
    Ramirez, Miranda
    Rush, Craig
    Stoops, William
    Lile, Joshua
    DRUG AND ALCOHOL DEPENDENCE, 2024, 260
  • [48] Dopamine Prediction Errors in Reward Learning and Addiction: From Theory to Neural Circuitry
    Keiflin, Ronald
    Janak, Patricia H.
    NEURON, 2015, 88 (02) : 247 - 263
  • [49] Correction to: Computing reward prediction errors and learning valence in the insect mushroom body
    James Bennett
    Thomas Nowotny
    BMC Neuroscience, 20
  • [50] Curiosity and Reward: Valence Predicts Choice and Information Prediction Errors Enhance Learning
    Marvin, Caroline B.
    Shohamy, Daphna
    JOURNAL OF EXPERIMENTAL PSYCHOLOGY-GENERAL, 2016, 145 (03) : 266 - 272