Original Article

Neuropsychopharmacology (2009) 34, 1649–1658; doi:10.1038/npp.2008.222; published online 17 December 2008

Neuroelectric Signatures of Reward Learning and Decision-Making in the Human Nucleus Accumbens

Michael X Cohen1,2, Nikolai Axmacher1, Doris Lenartz4, Christian E Elger1, Volker Sturm4 and Thomas E Schlaepfer3,5

  1. 1Department of Epileptology and Center for Life and Brain, University of Bonn, Bonn, Germany
  2. 2Department of Psychology, University of California, Davis, CA, USA
  3. 3Department of Psychiatry and Psychotherapy, University of Bonn, Bonn, Germany
  4. 4Department of Stereotactical Neurosurgery, University of Cologne, Cologne, Germany
  5. 5Department of Psychiatry, The Johns Hopkins University, Baltimore, MD, USA

Correspondence: Dr MX Cohen, Department of Epileptology and Center for Life and Brain, Sigmund-Freund-Str 25, Bonn 53105, Germany, Tel: 520-621-7086; Fax: 520-621-9306; E-mail: mikexcohen@gmail.com

Received 15 July 2008; Revised 3 November 2008; Accepted 9 November 2008; Published online 17 December 2008.

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Abstract

Learning that certain actions lead to risky rewards is critical for biological, social, and economic survival, but the precise neural mechanisms of such reward-guided learning remain unclear. Here, we show that the human nucleus accumbens plays a key role in learning about risks by representing reward value. We recorded electrophysiological activity directly from the nucleus accumbens of five patients undergoing deep brain stimulation for treatment of refractory major depression. Patients engaged in a simple reward-learning task in which they first learned stimulus-outcome associations (learning task), and then were able to choose from among the learned stimuli (choosing task). During the learning task, nucleus accumbens activity reflected potential and received reward values both during the cue stimulus and during the feedback. During the choosing task, there was no nucleus accumbens activity during the cue stimulus, but feedback-related activity was pronounced and similar to that during the learning task. This pattern of results is inconsistent with a prediction error response. Finally, analyses of cross-correlations between the accumbens and simultaneous recordings of medial frontal cortex suggest a dynamic interaction between these structures. The high spatial and temporal resolution of these recordings provides novel insights into the timing of activity in the human nucleus accumbens, its functions during reward-guided learning and decision-making, and its interactions with medial frontal cortex.

Keywords:

nucleus accumbens, risk-taking, reward, prediction error, intracranial EEG, motivation

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