Striatal activity and reward relativity: Neural signals encoding dynamic outcome valuation

Abstract

The striatum is a key brain region involved in reward processing. Striatal activity has been linked to encoding reward magnitude and integrating diverse reward outcome information. Recent work has supported involvement of striatum in the valuation of outcomes. The present work extends this idea by examining striatal activity during dynamic shifts in value that include different levels and directions of magnitude disparity. A novel task was utilized to produce diverse relative reward effects on a chain of instrumental action. Rats (rattus norvegicus) were trained to respond to cues associated with specific outcomes varying by food pellet magnitude. Animals were exposed to single outcome sessions followed by mixed outcome sessions and neural activity was compared between identical outcome trials from the different behavioral contexts. Results recording striatal activity show that neural responses to different task elements reflect incentive contrast as well as other relative effects that involve generalization between outcomes or possible influences of outcome variety. The activity most prevalent was linked to food consumption and post-consumption periods. Relative encoding was sensitive to magnitude disparity. A within-session analysis showed strong contrast effects dependent upon the outcome received in the immediately preceding trial. Significantly higher numbers of responses were found in ventral striatum linked to relative outcome effects. Our results support the idea that relative value can incorporate diverse relationships including comparisons from specific individual outcomes to general behavioral contexts. The striatum contains these diverse relative processes possibly enabling both a higher information yield concerning value shifts and a greater behavioral flexibility.

Significance Statement: This study is the initial research directly linking striatal activity to relative incentive contrast processes during instrumental action. The work not only demonstrates how striatal activity can dynamically encode specific outcome value information, but also shows that striatal activity simultaneously encodes value at different levels utilizing different types of information concerning the outcome and related context. The results link the neuroscience of reward to motivational theory that guides key experimental behavioral work on choice, decision-making and goal-directed action. Recent work has shown that mental illnesses such as schizophrenia and addiction are accompanied by deficits in reward valuation, and the present study provides key insight into neural processes that could be altered leading to emotional and behavioral impairments in mental disorders.