Modeling functions of striatal dopamine modulation in learning and planning.

Abstract

The activity of midbrain dopamine neurons is strikingly similar to the reward prediction error of temporal difference reinforcement learning models. Experimental evidence and simulation studies suggest that dopamine neuron activity serves as an effective reinforcement signal for learning of sensorimotor associations in striatal matrisomes. In the current study, we simulate dopamine neuron activity with the extended temporal difference model of Pavlovian learning and examine the influences of this signal on medium spiny neurons in striatal matrisomes. The modeled influences include transient membrane effects of dopamine D(1) receptor activation, dopamine-dependent long-term adaptations of corticostriatal transmission, and effects of dopamine on rhythmic fluctuations of the membrane potential between an elevated "up-state" and a hyperpolarized "down-state". The most dominant activity in the striatal matrisomes is assumed to elicit behaviors via projections from the basal ganglia to the thalamus and the cortex. This "standard model" performs successfully when tested for sensorimotor learning and goal-directed behavior (planning). To investigate the contributions of our model assumptions to learning and planning, we test the performance of several model variants that lack one of these mechanisms. These simulations show that the adaptation of the dopamine-like signal is necessary for sensorimotor learning and planning. Sensorimotor learning requires dopamine-dependent long-term adaptation of corticostriatal transmission. Lack of dopamine-like novelty responses decreases the number of exploratory acts, which impairs planning capabilities. The model loses its planning capabilities if the dopamine-like signal is simulated with the original temporal difference model, because the original temporal difference model does not form novel associative chains. Transient membrane effects of the dopamine-like signal on striatal firing substantially shorten the reaction time in the planning task. The capability for planning is improved by influences of dopamine on the durations of membrane potential fluctuations and by manipulations that prolong the reaction time of the model. These results suggest that responses of dopamine neurons to conditioned stimuli contribute to sensorimotor reward learning, novelty responses of dopamine neurons stimulate exploration, and transient dopamine membrane effects are important for planning.