Selective Theta-Synchronization of Choice-Relevant Information Subserves Goal-Directed Behavior

Theta activity reflects a state of rhythmic modulation of excitability at the level of single neuron membranes, within local neuronal groups and between distant nodes of a neuronal network. A wealth of evidence has shown that during theta states distant neuronal groups synchronize, forming networks of spatially confined neuronal clusters at specific time periods during task performance. Here, we show that a functional commonality of networks engaging in theta rhythmic states is that they emerge around decision points, reflecting rhythmic synchronization of choice-relevant information. Decision points characterize a point in time shortly before a subject chooses to select one action over another, i.e., when automatic behavior is terminated and the organism reactivates multiple sources of information to evaluate the evidence for available choices. As such, decision processes require the coordinated retrieval of choice-relevant information including (i) the retrieval of stimulus evaluations (stimulus–reward associations) and reward expectancies about future outcomes, (ii) the retrieval of past and prospective memories (e.g., stimulus–stimulus associations), (iii) the reactivation of contextual task rule representations (e.g., stimulus–response mappings), along with (iv) an ongoing assessment of sensory evidence. An increasing number of studies reveal that retrieval of these multiple types of information proceeds within few theta cycles through synchronized spiking activity across limbic, striatal, and cortical processing nodes. The outlined evidence suggests that evolving spatially and temporally specific theta synchronization could serve as the critical correlate underlying the selection of a choice during goal-directed behavior

A flexible mechanism of rule selection enables rapid feature-based reinforcement learning

Learning in a new environment is influenced by prior learning and experience. Correctly applying a rule that maps a context to stimuli, actions, and outcomes enables faster learning and better outcomes compared to relying on strategies for learning that are ignorant of task structure. However, it is often difficult to know when and how to apply learned rules in new contexts. In our study we explored how subjects employ different strategies for learning the relationship between stimulus features and positive outcomes in a probabilistic task context. We test the hypothesis that task naive subjects will show enhanced learning of feature specific reward associations by switching to the use of an abstract rule that associates stimuli by feature type and restricts selections to that dimension. To test this hypothesis we designed a decision making task where subjects receive probabilistic feedback following choices between pairs of stimuli. In the task, trials are grouped in two contexts by blocks, where in one type of block there is no unique relationship between a specific feature dimension (stimulus shape or colour) and positive outcomes, and following an un-cued transition, alternating blocks have outcomes that are linked to either stimulus shape or colour. Two-thirds of subjects (n=22/32) exhibited behaviour that was best fit by a hierarchical feature-rule model. Supporting the prediction of the model mechanism these subjects showed significantly enhanced performance in feature-reward blocks, and rapidly switched their choice strategy to using abstract feature rules when reward contingencies changed. Choice behaviour of other subjects (n=10/32) was fit by a range of alternative reinforcement learning models representing strategies that do not benefit from applying previously learned rules. In summary, these results show that untrained subjects are capable of flexibly shifting between behavioural rules by leveraging simple model-free reinforcement learning and context-specific selections to drive responses