Stochastic Dynamics Underlying Cognitive Stability and Flexibility

Cognitive stability and flexibility are core functions in the successful pursuit of behavioral goals. While there is evidence for a common frontoparietal network underlying both functions and for a key role of dopamine in the modulation of flexible versus stable behavior, the exact neurocomputational mechanisms underlying those executive functions and their adaptation to environmental demands are still unclear. In this work we study the neurocomputational mechanisms underlying cue based task switching (flexibility) and distractor inhibition (stability) in a paradigm specifically designed to probe both functions. We develop a physiologically plausible, explicit model of neural networks that maintain the currently active task rule in working memory and implement the decision process. We simplify the four-choice decision network to a nonlinear drift-diffusion process that we canonically derive from a generic winner-take-all network model. By fitting our model to the behavioral data of individual subjects, we can reproduce their full behavior in terms of decisions and reaction time distributions in baseline as well as distractor inhibition and switch conditions. Furthermore, we predict the individual hemodynamic response timecourse of the rule-representing network and localize it to a frontoparietal network including the inferior frontal junction area and the intraparietal sulcus, using functional magnetic resonance imaging. This refines the understanding of task-switch-related frontoparietal brain activity as reflecting attractor-like working memory representations of task rules. Finally, we estimate the subject-specific stability of the rule-representing attractor states in terms of the minimal action associated with a transition between different rule states in the phase-space of the fitted models. This stability measure correlates with switching-specific thalamocorticostriatal activation, i.e., with a system associated with flexible working memory updating and dopaminergic modulation of cognitive flexibility. These results show that stochastic dynamical systems can implement the basic computations underlying cognitive stability and flexibility and explain neurobiological bases of individual differences.Author Summary: In this work we develop a neurophysiologically inspired dynamical model that is capable of solving a complex behavioral task testing cognitive stability and flexibility. We can individually fit the behavior of each of 20 human subjects that conducted this stability-flexibility task during functional magnetic resonance imaging (fMRI). The physiological nature of our model allows us to estimate the energy consumption of the rule-representing module, which we use to predict the hemodynamic fMRI response. Through this model-based prediction, we localize the rule module to a frontoparietal network known to be required for cognitive stability and flexibility. In this way we both validate our model, which is based on noisy attractor dynamics, and specify the computational role of a cortical network that is well-established in human neuroimaging research. Additionally, we quantify the individual stability of the rule-representing states and relate this stability to individual differences in energy consumption during task switching versus distractor inhibition. Hereby we show that the activation of a thalamocorticostriatal network involved in the dopaminergic modulation of cognitive stability is modulated by the model-derived stability of the frontoparietal rule-representing network. Altogether, we show that noisy dynamic systems are likely to implement the basic computations underlying cognitive stability and flexibility.