Selection of actions in the basal ganglia-thalamocortical circuits: review and model

Abstract

The paper reviews the 20-year experience of recording impulse activity of neurons in the basal ganglia-thalamocortical circuits. These recordings were made from patients with Parkinson's disease who failed to respond to conventional medical treatment and who had undergone stereotaxic neurosurgery. When taken together, the results show that: (1) the basal ganglia-thalamocortical circuits become active only when a stimulus is attended or when a movement is voluntarily implemented, i.e. they are involved in the process of selection of an appropriate sensory stimulus for advanced processing and in the process of selection of an appropriate motor action for achieving a certain goal; (2) neuronal circuits responsible for assessment actions and for motor acts are segregated; (3) inhibitory opponent neuronal mechanisms are implemented for initiating and suppressing inappropriate actions; and (4) preparation to make different assessment actions (attentional set) is associated with different preparatory activities. To explain these findings a hypothesis of action programming has been formulated. According to it, the whole of human behavior is divided into separate sensory-motor-cognitive actions, while the brain in turn is divided into separate systems playing different roles in the organization of actions. The system for action selection that includes the basal ganglia-thalamic circuits plays a critical role in initiation of, preparation for, and suppression of these actions. The neuronal mechanisms for the system for action selection including mapping of actions, 'winner takes all' operations in the striatum, disinhibition and inhibition process in the thalamus are suggested and discussed.