Substantial evidence suggests that the phasic activities of dopaminergic neurons in the primate midbrain represent a temporal difference (TD) error in predictions of future reward, with increases above and decreases below baseline consequent on positive and negative prediction errors, respectively. However, dopamine cells have very low baseline activity, which implies that the representation of these two sorts of error is asymmetric. We explore the implications of this seemingly innocuous asymmetry for the interpretation of dopaminergic firing patterns in experiments with probabilistic rewards which bring about persistent prediction errors. In particular, we show that when averaging the non-stationary prediction errors across trials, a ramping in the activity of the dopamine neurons should be apparent, whose magnitude is dependent on the learning rate. This exact phenomenon was observed in a recent experiment, though being interpreted there in antipodal terms as a within-trial encoding of uncertainty.
Reinforcement learning models have long promised to unify computa- tional, psychological and neural accounts of appetitively conditioned be- havior. However, the bulk of data on animal conditioning comes from free-operant experiments measuring how fast animals will work for rein- forcement. Existing reinforcement learning (RL) models are silent about these tasks, because they lack any notion of vigor. They thus fail to ad- dress the simple observation that hungrier animals will work harder for food, as well as stranger facts such as their sometimes greater produc- tivity even when working for irrelevant outcomes such as water. Here, we develop an RL framework for free-operant behavior, suggesting that subjects choose how vigorously to perform selected actions by optimally balancing the costs and benefits of quick responding. Motivational states such as hunger shift these factors, skewing the tradeoff. This accounts normatively for the effects of motivation on response rates, as well as many other classic findings. Finally, we suggest that tonic levels of dopamine may be involved in the computation linking motivational state to optimal responding, thereby explaining the complex vigor-related ef- fects of pharmacological manipulation of dopamine.
A broad range of neural and behavioral data suggests that the brain contains multiple systems for behavioral choice, including one associated with prefrontal cortex and another with dorsolateral striatum. However, such a surfeit of control raises an additional choice problem: how to arbitrate between the systems when they disagree. Here, we consider dual-action choice systems from a normative perspective, using the computational theory of reinforcement learning. We identify a key trade-off pitting computational simplicity against the flexible and statistically efficient use of experience. The trade-off is realized in a competition between the dorsolateral striatal and prefrontal systems. We suggest a Bayesian principle of arbitration between them according to uncertainty, so each controller is deployed when it should be most accurate. This provides a unifying account of a wealth of experimental evidence about the factors favoring dominance by either system.
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