Real-time updates to behavioral strategy require animals to understand how many actions have been executed toward completion of a goal. These operations are essential for optimizing behavior and have been linked to dopaminergic innervation of prefrontal cortex networks (Gallistel and Gibbon, 2000; Allman et al., 2011; Lustig, 2011). It is an open question how networks of dopaminergic and non-dopaminergic neurons in the ventral tegmental area (VTA) encode information when multiple or complex behaviors are required to earn rewards (Niv et al., 2006; Dayan and Niv, 2008; Niv and Schoenbaum, 2008). Most electrophysiological studies have focused on the averaged activity of dopamine neurons during reward prediction error signaling in simple behavioral paradigms. Thus, VTA neuronal correlates of executive processes and complex behavior remain elusive.
In the current experiment, rats learned to repetitively execute actions (nose pokes) to receive rewarding outcomes (sugar pellets). These actions were randomly rewarded, and all actions were identically valued because each was equally likely to be reinforced. Actions differed only by their number within a trial. While animals executed serial actions, many VTA neurons were activated or suppressed by unique subsets of actions within a trial. Some neurons fired preferentially during low numbered actions while others preferred high numbered actions. A population averaging approach, which is conventionally used for analysis of dopaminergic neuronal activity, offered poor decoding of action number. In contrast, action number within a trial was accurately decoded from the entire pool of unique activity patterns, considering each neuron independently. These results suggest that the collective activity of VTA neuronal ensembles signals real-time information about ongoing action number—a critical component of behavioral organization
