Modulation of Tonically Active Neurons of the Monkey Striatum by Events Carrying Different Force and Reward Information.

The role of basal ganglia in motivational processes has been under scrutiny in recent decades, with increasing evidence from clinical studies of cognitive and motivational deficits in patients with basal ganglia lesions. Tonically active neurons (TANs), the presumed striatal cholinergic interneurons, could be important actors in integrating and relaying motivational information arising from various modalities. Their multiphasic responses to rewards and to conditioned stimuli associated with reward conferred them a role in limbic processes. They are also modulated by a task's motor aspect. Recent studies suggest they are influenced by the context in which behavioral responses are expressed. To investigate the role of TANs in motor-limbic interaction processes, we recorded 169 TANs in the striatum of two monkeys performing a motivational task, in which they had to develop a variable force to receive different amounts of reward in response to visual stimuli. Our results reveal new features of TANs response properties. First, TANs usually responded either by a pause or an elevation of discharge rate to the visual cues and the reward, with few neurons combining both pause and rebound. Second, the elevations of discharge rate after the cues were most sensitive to the least valuable (high force or small reward) task conditions. Finally, the responses of TANs to the visual cues were time locked on the onset of the animal's movement. TANs' population and responses could thus play a role in signaling less attractive situations, those with either a high motor demand and/or small reward. SIGNIFICANCE STATEMENT: Tonically active neurons (TANs) are known for their responses to unpredictable positive or negative events. However, here we show that TANs respond by a pause or an increase in their activity to all rewarding events in a task in which combined visual cues indicate to the monkeys the levels of force to produce and the upcoming reward. Unlike the pause, the increase in activity is modulated by task parameters and is most sensitive to the least attractive task conditions (high force and/or small reward). TANs' responses triggered by cue occurrence are also modulated by movement-related information (movement onset). We therefore propose here that TANs could play a role, via their action on striatal projections neurons, in maintaining high cost/low benefit ratio behaviors.