Towards an executive without a homunculus: computational models of the prefrontal cortex/basal ganglia system

The prefrontal cortex (PFC) has long been thought to serve as an ‘executive’ that controls the selection of actions and cognitive functions more generally. However, the mechanistic basis of this executive function has not been clearly specified often amounting to a homunculus. This paper reviews recent attempts to deconstruct this homunculus by elucidating the precise computational and neural mechanisms underlying the executive functions of the PFC. The overall approach builds upon existing mechanistic models of the basal ganglia (BG) and frontal systems known to play a critical role in motor control and action selection, where the BG provide a ‘Go’ versus ‘NoGo’ modulation of frontal action representations. In our model, the BG modulate working memory representations in prefrontal areas to support more abstract executive functions. We have developed a computational model of this system that is capable of developing human-like performance on working memory and executive control tasks through trial-and-error learning. This learning is based on reinforcement learning mechanisms associated with the midbrain dopaminergic system and its activation via the BG and amygdala. Finally, we briefly describe various empirical tests of this framework.