fMRI and electrophysiological responses in the Anterior Cingulate Cortex of Monkeys engaged in value-based decision making

Elsewhere at this meeting we present functional magnetic resonance imaging (fMRI) measurements in both monkey and human subjects performing a simple value-based decision making task. These data reveal a correspondence in the network of brain areas activated in the two species in this foraging task. Most interesting among these are areas whose fMRI BOLD signal correlates with variations in local reward rate, a task variable known to account for variability in behavioral choices and neural activity in similar games (e.g. Sugrue et al, Science, 2004). In particular, the Anterior Cingulate Cortex (ACC) in both species showed strong local reward rate modulation. These fMRI results prompted us to record from single neurons in monkey ACC in a similar foraging task. Preliminary results from these experiments confirm that ACC neurons are strongly modulated in this task, with individual cells encoding a variety of task related signals. These include a prelude response that peaks prior to option selection and scales with local reward rate, and responses related to two highly salient task events - the delivery of rewards, and the decision to switch between the competing reward sources. Interestingly, a majority of neurons recorded to date respond to rewards with a decrease in their firing rate, and show a negative encoding of local reward rate. We compare the sign and time course of these electrophysiological responses with those of the corresponding BOLD signal. Several theories have emphasized a specific role for ACC in the processing and prediction of errors and conflict (e.g. Brown Braver, Science, 2005). More recently, this emphasis has been challenged and a more general role for ACC suggested, in which it integrates both errors and rewards over time to develop a representation of the value of competing options (Kennerley et al., Nat. Neurosci., 2006). In our task, subjects must forage for rewards in a dynamic and probabilistic environment where there are no 'correct' or 'error' responses. Our finding that BOLD and single unit responses in the ACC are modulated by local reward rate in this task is consistent with a more general conception of ACC function. Moreover, the high proportion of ACC neurons that exhibit a negative encoding of reward and reward rate may explain why error processing has been overemphasized in earlier accounts of ACC activation. This work demonstrates that fMRI and electrophysiology in the awake behaving monkey provide complementary tools for identifying and investigating the neural signals responsible for value-based decision making and suggest the utility of this combined approach in studying similar complex cognitive phenomena