Differential contributions of the globus pallidus and ventral thalamus to stimulus-response learning in humans

The ability to learn associations between stimuli, responses and rewards is a prerequisite for survival. Models of reinforcement learning suggest that the striatum, a basal ganglia input nucleus, vitally contributes to these learning processes. Our recently presented computational model predicts, first, that not only the striatum, but also the globus pallidus contributes to the learning (i.e., exploration) of stimulus-response associations based on rewards. Secondly, it predicts that the stable execution (i.e., exploitation) of well-learned associations involves further learning in the thalamus. To test these predictions, we postoperatively recorded local field potentials (LFPs) from patients that had undergone surgery for deep brain stimulation to treat severe movement disorders. Macroelectrodes were placed either in the globus pallidus or in the ventral thalamus. During recordings, patients performed a reward-based stimulus-response learning task that comprised periods of exploration and exploitation. We analyzed correlations between patients' LFP amplitudes and model-based estimates of their reward expectations and reward prediction errors. In line with our first prediction, pallidal LFP amplitudes during the presentation of rewards and reward omissions correlated with patients' reward prediction errors, suggesting pallidal access to reward-based teaching signals. Unexpectedly, the same was true for the thalamus. In further support of this prediction, pallidal LFP amplitudes during stimulus presentation correlated with patients' reward expectations during phases of low reward certainty - suggesting pallidal participation in the learning of stimulus-response associations. In line with our second prediction, correlations between thalamic stimulus-related LFP amplitudes and patients' reward expectations were significant within phases of already high reward certainty, suggesting thalamic participation in exploitation.