Encoding by Response Duration in the Basal Ganglia

Several models have suggested that information transmission in the basal ganglia (BG) involves gating mechanisms, where neuronal activity modulates the extent of gate aperture and its duration. Here, we demonstrate that BG response duration is informative about a highly abstract stimulus feature and show that the duration of “gate opening” can indeed be used for information transmission through the BG. We analyzed recordings from three BG locations: the external part of the globus pallidus (GPe), the substantia nigra pars reticulata (SNr), and dopaminergic neurons from the substantia nigra pars compacta (SNc) during performance of a probabilistic visuomotor task. Most (>85%) of the neurons showed significant rate modulation following the appearance of cues predicting future reward. Trial-to-trial mutual information analysis revealed that response duration encoded reward prospects in many (42%) of the responsive SNr neurons, as well as in the SNc (26.9%), and the GPe (29.3%). Whereas the low-frequency discharge SNc neurons responded with only an increase in firing rate, SNr and GPe neurons with high-frequency tonic discharge responded with both increases and decreases. Conversely, many duration-informative neurons in SNr (68%) and GPe (50%) responded with a decreased rather than an increased rate. The response duration was more informative than the extreme (minimal or maximal) amplitude or spike count in responsive bins of duration-informative neurons. Thus response duration is not simply correlated with the discharge rate and can provide additional information to the target structures of the BG.

Activity of Primate Orbitofrontal and Dorsolateral Prefrontal Neurons: Effect of Reward Schedule on Task-related Activity

Recent studies show that task-related activity in the dorsolateral prefrontal cortex (DLPFC) is modulated by the quality and quantity of the reward, suggesting that the subject's motivational state affects cognitive operations in the DLPFC. The orbito-frontal cortex (OFC) is a possible source of motivational inputs to the DLPFC. However, it is not well known whether these two areas exhibit similar motivational effects on task-related activity. We compared motivational effects on task-related activity in these areas while a monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, reward was given only after the successful completion of four consecutive trials, whereas in the ODR-2 schedule, reward was given after every correct trial. Task-related activities in both areas showed spatial selectivity. The spatial characteristics of task-related activity remained constant in both schedules. Task-related activity in both areas, especially delay-period activity, was also affected by the reward schedule and the magnitude of the activity gradually increased depending on the proximity of the reward trial in the ODR-1 schedule. More task-related OFC activities were affected by reward schedules, whereas more task-related DLPFC activities were affected by spatial factors and reward schedules. These results indicate that the OFC plays a role in monitoring the proximity of the reward trial and detecting reward delivery, whereas the DLPFC plays a role in performing cognitive operations and integrating cognitive and motivational information. These results also indicate that spatial information and the animal's motivational state independently affect neuronal activity in both areas.

History- and Current Instruction-Based Coding of Forthcoming Behavioral Outcomes in the Striatum

Animals optimize behaviors by predicting future critical events based on histories of actions and their outcomes. When behavioral outcomes like reward and aversion are signaled by current external cues, actions are directed to acquire the reward and avoid the aversion. The basal ganglia are thought to be the brain locus for reward-based adaptive action planning and learning. To understand the role of striatum in coding outcomes of forthcoming behavioral responses, we addressed two specific questions. First, how are the histories of reward and aversion used for encoding forthcoming outcomes in the striatum during a series of instructed behavioral responses? Second, how are the behavioral responses and their instructed outcomes represented in the striatum? We recorded discharges of 163 presumed projection neurons in the striatum while monkeys performed a visually instructed lever-release task for reward, aversion, and sound outcomes, whose occurrences could be estimated by their histories. Before outcome instruction, discharge rates of a subset of neurons activated in this epoch showed positive or negative regression slopes with reward history (24/44), that is, to the number of trials since the last reward trial, which changed in parallel with reward probability of current trials. The history effect was also observed for the aversion outcome but in far fewer neurons (3/44). Once outcomes were instructed in the same task, neurons selectively encoded the outcomes before and after behavioral responses (reward, 46/70; aversion, 6/70; sound, 6/70). The history- and current instruction–based coding of forthcoming behavioral outcomes in the striatum might underlie outcome-oriented behavioral modulation.