Neurophysiology of Reward-Guided Behavior: Correlates Related to Predictions, Value, Motivation, Errors, Attention, and Action

Abstract

Many brain areas are activated by the possibility and receipt of reward. Are all of these brain areas reporting the same information about reward? Or are these signals related to other functions that accompany reward-guided learning and decision-making? Through carefully controlled behavioral studies, it has been shown that reward-related activity can represent reward expectations related to future outcomes, errors in those expectations, motivation, and signals related to goal- and habit-driven behaviors. These dissociations have been accomplished by manipulating the predictability of positively and negatively valued events. Here, we review single neuron recordings in behaving animals that have addressed this issue. We describe data showing that several brain areas, including orbitofrontal cortex, anterior cingulate, and basolateral amygdala signal reward prediction. In addition, anterior cingulate, basolateral amygdala, and dopamine neurons also signal errors in reward prediction, but in different ways. For these areas, we will describe how unexpected manipulations of positive and negative value can dissociate signed from unsigned reward prediction errors. All of these signals feed into striatum to modify signals that motivate behavior in ventral striatum and guide responding via associative encoding in dorsolateral striatum.

Development and function of the midbrain dopamine system: what we know and what we need to

“…Unlike neural activity in VTA, the activity of SNc mdDA neurons might play a more critical role in signaling salience (Kakade & Dayan ; Matsumoto & Hikosaka ), signaling when outcomes are unexpected, either positively or negatively. This salience signal could play an additional critical role in learning, making cues associated with the previous action more salient (Bissonette & Roesch ; Bromberg‐Martin et al ; Redgrave & Gurney ; Redgrave et al ). Thus, the combination of mdDA neurons in SNc signaling salience after unexpected outcomes and mdDA neurons from VTA assigning the value of the unexpected outcome (positive or negative) may represent a complementary and powerful approach to learning (Fig.…”

Value and choice as separable, stable representations in orbitofrontal cortex

“…Value-based decision-making is an essential component of behavior, and its neural basis has been an area of intense scientific inquiry [1][2][3] . Economists, psychologists and neuroscientists have long-posited a need for separable representations of key decision variables-including 1) initial valuation of the offer, 2) chosen action, and 3) expected outcome given the choice-that in turn support respective steps in the decision process: 1) committing to an initial behavioral policy, 2) computing expected outcome while executing the policy and then later assigning credit to the chosen action, and 3) reevaluating the policy mid-execution and then later comparing expected and received outcomes to update future expectations 4 .…”

Neurophysiology of rule switching in the corticostriatal circuit

“…The mPFC has robust projections to medial dorsal striatum (mDS), constituting 15% of all mPFC efferent projections(Gabbott et al, 2005). The mDS is known to encode the relationships between stimuli and responses, the direction of impending movements, and the associations between response and outcomes(Ragozzino et al, 2002, Pasupathy and Miller, 2005, Balleine et al, 2007, Balleine et al, 2009, Kimchi and Laubach, 2009, Balleine and O'Doherty, 2010, van der Meer et al, 2010, Hilario et al, 2012, Bissonette and Roesch, 2015b). Recently, these mPFC projections to striatal striosomes has been manipulated optogenetically, demonstrating a causal role for cortical – especially mPFC – projections to striatum influencing cost-benefit decision making(Friedman et al, 2015).…”