Frontostriatal Contribution to the Interplay of Flexibility and Stability in Serial Prediction

Abstract

Surprising events may be relevant or irrelevant for behavior, requiring either flexible adjustment or stabilization of our model of the world and according response-strategies. Cognitive flexibility and stability in response to environmental demands have been described as separable cognitive states, associated with activity of striatal and lateral prefrontal regions, respectively. It so far remains unclear, however, whether these two states act in an antagonistic fashion, and which neural mechanisms mediate the selection of respective responses on the one hand, and a transition between these states on the other. In the present study, we tested whether the functional dichotomy between striatal and prefrontal activity applies for the separate functions of updating (in response to changes in the environment, i.e., switches) and shielding (in response to chance occurrences of events violating expectations, i.e., drifts) of current predictions. We measured brain activity using functional magnetic resonance imaging (fMRI) while twenty healthy subjects performed a task which required to serially predict upcoming items. Switches between predictable sequences had to be indicated via button press while sequence omissions (drifts) had to be ignored. We further varied the probability of switches and drifts to assess the neural network supporting the transition between flexible and stable cognitive states as a function of recent performance history in response to environmental demands. While flexible switching between models was associated with activation in medial prefrontal cortex (PFC; BA 9 & 10), we found that stable maintenance of the internal model corresponded to activation in the lateral PFC (BA 6 & IFG). Our findings extend previous studies on the interplay of flexibility and stability suggesting that different prefrontal regions are activated by different types of prediction errors, dependent on their behavioral requirements. Furthermore, we found that striatal activation in response to switches and drifts was modulated by participants’ successful behavior towards these events suggesting the striatum to be responsible for response selections following unpredicted stimuli. Finally, we observed that the dopaminergic midbrain modulates the transition between different cognitive states, thresholded by participants’ individual performance history in response to temporal environmental demands.