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

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.

Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Response to commentary

“…In contrast, Cohen et al cite work from their group (Cohen et al (2009) in which they find only weak correlations between scalp-recorded ERPs and depth recordings from the basal ganglia during a reward learning task. Examining the scalp-recorded ERPs presented in the supplementary data section, however, suggests that unfavorable compared to favorable outcomes did not elicit an FN in the group of patients studied by Cohen et al Following reward feedback, there was a positivity to losses and a negativity to gains, a pattern which is nearly opposite to the existing literature on the FN.…”

The Reward Circuit: Linking Primate Anatomy and Human Imaging

“…A recent meta-analysis of over 20 similar FMRI studies has confirmed preferential activation of the NAcc during anticipation of monetary gains, but not during anticipation of losses (Knutson and Greer, 2008). Depthelectrode recordings of epileptic patients gambling have also shown that NAcc activity increases proportional to the magnitude of anticipated reward (Cohen et al, 2009a). This proportional response to anticipated reward magnitude provided an anchor for exploring the impact of varying other attributes of anticipated reward.…”

Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Temporospatial principal components analysis and source localization of the feedback negativity: Commentary

“…These neurons do not have a geometrically parallel organization like cortical pyramidal cells; it is therefore unlikely that dendritic potentials from the striatum could propagate to the scalp. Indeed, empirical measures of synchrony between the human ventral striatum and surface EEG is at best 0.2 (on a scale from 0 to 1) (Cohen et al, 2009). More importantly, maximal correlation is temporally lagged such that ventral striatal and scalprecorded EEG signals do not occur simultaneously.…”