Academic journal article Cognitive, Affective and Behavioral Neuroscience

Expectations, Gains, and Losses in the Anterior Cingulate Cortex

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Expectations, Gains, and Losses in the Anterior Cingulate Cortex

Article excerpt

The anterior cingulate cortex (ACC) participates in evaluating actions and outcomes. Little is known on how action-reward values are processed in ACC and if the context in which actions are performed influences this processing. In the present article, we report ACC unit activity of monkeys performing two tasks. The first task tested whether the encoding of reward values is context dependent-that is, dependent on the size of the other rewards that are available in the current block of trials. The second task tested whether unexpected events signaling a change in reward are represented. We show that the context created by a block design (i.e., the context of possible alternative rewards) influences the encoding of reward values, even if no decision or choice is required. ACC activity encodes the relative and not absolute expected reward values. Moreover, cingulate activity signals and evaluates when reward expectations are violated by unexpected stimuli, indicating reward gains or losses.

Decisions rely on the estimation of the outcome that one will get after a choice is made and an action performed. This estimation, the expected value, is based on the representations of expected and obtained rewards-and more generally, outcomes-that are associated with objects or act through learning (Lee & Seo, 2007). Value is affected by time of occurrence, probability, frequency, valence, and size of rewards. The ensemble of alternative outcomes available in the current environment can also have an effect on expected values.

The processing of rewards involves a so-called reward system, a network of brain structures including the orbitofrontal cortex (OFC), the ventral striatum, and the mesencephalic dopaminergic system and the anterior cingulate cortex (ACC; Schultz, 2000). OFC activity is modulated by expected outcomes and reflects the relative values assigned by the animals to alternative choices (PadoaSchioppa & Assad, 2006). Encoding of reward values by dopaminergic neurons is adaptive and relative to the potential outcomes (Tobler, Fiorillo, & Schultz, 2005). Within the reward system, the ACC has a particular position. Its role most likely consists of building outcome-action associations that serve to elaborate with experience the expected value of particular decisions (Kennerley, Walton, Behrens, Buckley, & Rushworth, 2006; Rushworth, Walton, Kennerley, & Bannerman, 2004). There is evidence that the ACC is involved in representing expected values (Amiez, Joseph, & Procyk, 2006). Thus, one can also expect relative coding of reward values in the ACC.

ACC function also encompasses the voluntary selection of behavior and positive and negative outcome evaluations (Amiez, Joseph, & Procyk, 2005; Shima & Tanji, 1998; Walton, Devlin, & Rushworth, 2004). Several theories are proposed to explain ACC activation in humans during tasks that involve active performance monitoring (Holroyd & Coles, 2002; Kerns et al., 2004; Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004; Rushworth et al., 2004). Signals from ACC have been interpreted in terms of the detection of conflict in processing competitive representations-for example, alternative action plans (Botvinick, Cohen, & Carter, 2004). These ACC signals could also possibly reflect detection of events at odds with expectations, especially in terms of rewards (Gehring & Willoughby, 2002; Holroyd & Coles, 2002; Rushworth et al., 2004). Indeed, ACC feedback-related activity varies with reward prediction errors during learning (Amiez et al., 2005; Holroyd & Coles, 2002; Matsumoto, Matsumoto, Abe, & Tanaka, 2007).

The present experiments were designed to further investigate the representations of expected values. We report recordings in the ACC of monkeys performing two tasks: the scaled-reward task, and the expect task that involved neither making a decision between alternative choices nor learning particular reward values. …

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