Complex population response of dorsal putamen neurons predicts the ability to learn

PLoS One. 2013 Nov 14;8(11):e80683. doi: 10.1371/journal.pone.0080683. eCollection 2013.


Day-to-day variability in performance is a common experience. We investigated its neural correlate by studying learning behavior of monkeys in a two-alternative forced choice task, the two-armed bandit task. We found substantial session-to-session variability in the monkeys' learning behavior. Recording the activity of single dorsal putamen neurons we uncovered a dual function of this structure. It has been previously shown that a population of neurons in the DLP exhibits firing activity sensitive to the reward value of chosen actions. Here, we identify putative medium spiny neurons in the dorsal putamen that are cue-selective and whose activity builds up with learning. Remarkably we show that session-to-session changes in the size of this population and in the intensity with which this population encodes cue-selectivity is correlated with session-to-session changes in the ability to learn the task. Moreover, at the population level, dorsal putamen activity in the very beginning of the session is correlated with the performance at the end of the session, thus predicting whether the monkey will have a "good" or "bad" learning day. These results provide important insights on the neural basis of inter-temporal performance variability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Learning / physiology*
  • Macaca mulatta
  • Neurons / cytology*
  • Neurons / physiology*
  • Putamen / cytology*
  • Putamen / physiology

Grants and funding

This study was partly supported by the Franco-Israeli Neuroscience Lab administered by the CNRS, the HUJI, the University of Bordeaux and the University Paris VI- Descartes; a grant from the Ministry of Science, Culture & Sport, Israel, and the Ministry of Research, France and by the Programme Interdisciplinaire NeuroInformatique administered by the CNRS. S.L. was supported by a France-Parkinson foundation grant. Y.L. was supported by the Israel Science Foundation (grant No. 868/08). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.