Signatures of Value Comparison in Ventral Striatum Neurons

RESEARCH ARTICLE Signatures of Value Comparison in Ventral Striatum Neurons Caleb E. Strait1*, Brianna J. Sleezer1,2, Benjamin Y. Hayden1 1 Department of Brain and Cognitive Sciences and Center for Visual Science, University of Rochester, Rochester, New York, United States of America, 2 Neuroscience Graduate Program, University of Rochester, Rochester, New York, United States of America * Abstract OPEN ACCESS Citation: Strait CE, Sleezer BJ, Hayden BY (2015) Signatures of Value Comparison in Ventral Striatum Neurons. PLoS Biol 13(6): e1002173. doi:10.1371/ journal.pbio.1002173 Academic Editor: Matthew F. S. Rushworth, Oxford University, UNITED KINGDOM Received: July 23, 2014 The ventral striatum (VS), like its cortical afferents, is closely associated with processing of rewards, but the relative contributions of striatal and cortical reward systems remains unclear. Most theories posit distinct roles for these structures, despite their similarities. We compared responses of VS neurons to those of ventromedial prefrontal cortex (vmPFC) Area 14 neurons, recorded in a risky choice task. Five major response patterns observed in vmPFC were also observed in VS: (1) offer value encoding, (2) value difference encoding, (3) preferential encoding of chosen relative to unchosen value, (4) a correlation between residual variance in responses and choices, and (5) prominent encoding of outcomes. We did observe some differences as well; in particular, preferential encoding of the chosen option was stronger and started earlier in VS than in vmPFC. Nonetheless, the close match between vmPFC and VS suggests that cortex and its striatal targets make overlapping contributions to economic choice. Accepted: May 8, 2015 Published: June 18, 2015 Copyright: © 2015 Strait et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available on figshare (http://figshare.com/articles/Data_for_ Signatures_of_value_comparison_in_ventral_ striatum_neurons_/1332487). Funding: This research was supported by a National Institutes of Health http://grants.nih.gov/grants/oer. htm R01 (DA038106) and a NARSAD Young Investigator Reward from the Brain and Behavior Research Foundation http://bbrfoundation.org/ to BYH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author Summary The neural calculations underlying reward-based choice are closely associated with a network of brain areas including the ventral striatum (VS) and ventromedial prefrontal cortex (vmPFC). Most theories ascribe distinct roles to these two structures during choice, but these differences have yet to be confirmed at the level of single neurons. We compared responses of VS neurons to those of vmPFC neurons recorded in rhesus macaques choosing between potential gambles for water rewards. We found widespread similarities in the way that VS and vmPFC neurons fire during the choice process. Neurons in both areas encoded the value of the offered gamble, the difference in value between offered gambles, and the gamble outcome. Additionally, both areas showed stronger coding for the chosen gamble than for the unchosen one and predicted choice even when we controlled for offer value. Interestingly, preferential encoding of the chosen option was stronger and started earlier in VS than in vmPFC. Nonetheless, similarities between vmPFC and VS suggest that cortex and its striatal targets make overlapping contributions to reward-based choice. PLOS Biology | DOI:10.1371/journal.pbio.1002173 June 18, 2015 1 / 22 Signatures of Value Comparison in Ventral Striatum Neurons Competing Interests: The authors have declared that no competing interests exist. Abbreviations: dACC, dorsal anterior cingulate cortex; FSI, fast-spiking interneuron; MSN, medium spiny neuron; OFC, orbitofrontal cortex; PCC, posterior cingulate cortex; RPE, reward prediction error; vmPFC, ventromedial prefrontal cortex; VS, ventral striatum. Introduction Making beneficial choices about rewarding options is a major function of our brains and is critical for our survival. Consequently, understanding the mechanisms of reward-based choice is a major goal of psychology, microeconomics, animal behavior, and psychiatry [1–7]. Recent empirical and theoretical work has begun to uncover the basic underpinnings of reward-based choice (reviewed in [8–11]). Research into this topic is directly inspired by the success of the perceptual decision-making research program [12,13]. One reason why we currently lack a correspondingly detailed understanding of reward-based choice is that the full set of brain structures involved in this process, and their specific functions, has yet to be established. In particular, it remains unclear whether reward-based choice takes place in a single core structure that has a dedicated value comparison function, or whether it occurs more broadly, as comparison steps are implemented in unison across different brain regions [14]. Among brain regions associated with reward-based choice, we are particularly interested in the ventral striatum (VS) and the ventromedial prefrontal cortex (vmPFC) [15]. Both regions are associated with option evaluation and with value comparison in neuroimaging and lesion studies [16– 24]. On the one hand, this similarity in response properties suggests that they may play similar roles in reward-based choice. On the other hand, much evidence points to distinct roles for the vmPFC and VS. Specifically, VS, like other striatal regions, is generally linked to learning, including habit learning, and to action selection, while vmPFC, like other prefrontal regions, is associated with executive control and flexible, online regulation of behavior [25–40]. Of course, there is a sizable literature on the contributions of ventral striatum to reward-based choice, including action selection [37–40]. These include learning, or action-selection–centered approaches (e.g., actor-critic models, in which VS learns to predict future rewards, while PFC formulates a choice policy designed to maximize reward [41,42]), and gating or modulation theories, wherein the ventral striatum facilitates motor plans by disinhibiting motor plans [43,44]. Indeed, one recent paper found value coding in VS precedes choice but only follows choice in orbitofrontal cortex (OFC; a structure that is adjacent to vmPFC), suggesting that it is VS, and not cortex, that directs the choice [45]. One common trend among these models is that they generally attribute ventral striatum and cortical areas different, and generally complementary, functions. The different roles assigned to cortical and striatal reward signals may reflect true functional differences between these areas, but it is diffic (...truncated)