Eligibility Traces and Plasticity on Behavioral Time Scales: Experimental Support of neoHebbian Three-Factor Learning Rules

Most elementary behaviors such as moving the arm to grasp an object or walking into the next room to explore a museum evolve on the time scale of seconds; in contrast, neuronal action potentials occur on the time scale of a few milliseconds. Learning rules of the brain must therefore bridge the gap between these two different time scales. Modern theories of synaptic plasticity have postulated that the co-activation of pre- and postsynaptic neurons sets a flag at the synapse, called an eligibility trace, that leads to a weight change only if an additional factor is present while the flag is set. This third factor, signaling reward, punishment, surprise, or novelty, could be implemented by the phasic activity of neuromodulators or specific neuronal inputs signaling special events. While the theoretical framework has been developed over the last decades, experimental evidence in support of eligibility traces on the time scale of seconds has been collected only during the last few years. Here we review, in the context of three-factor rules of synaptic plasticity, four key experiments that support the role of synaptic eligibility traces in combination with a third factor as a biological implementation of neoHebbian three-factor learning rules

Learning in Volatile Environments With the Bayes Factor Surprise

Surprise-based learning allows agents to rapidly adapt to nonstationary stochastic environments characterized by sudden changes. We show that exact Bayesian inference in a hierarchical model gives rise to a surprise-modulated trade-off between forgetting old observations and integrating them with the new ones. The modulation depends on a probability ratio, which we call the Bayes Factor Surprise, that tests the prior belief against the current belief. We demonstrate that in several existing approximate algorithms, the Bayes Factor Surprise modulates the rate of adaptation to new observations. We derive three novel surprise-based algorithms, one in the family of particle filters, one in the family of variational learning, and one in the family of message passing, that have constant scaling in observation sequence length and particularly simple update dynamics for any distribution in the exponential family. Empirical results show that these surprise-based algorithms estimate parameters better than alternative approximate approaches and reach levels of performance comparable to computationally more expensive algorithms. The Bayes Factor Surprise is related to but different from the Shannon Surprise. In two hypothetical experiments, we make testable predictions for physiological indicators that dissociate the Bayes Factor Surprise from the Shannon Surprise. The theoretical insight of casting various approaches as surprise-based learning, as well as the proposed online algorithms, may be applied to the analysis of animal and human behavior and to reinforcement learning in nonstationary environments

Evidence for eligibility traces in human learning

Whether we prepare a coffee or navigate to a shop: in many tasks we make multiple decisions before reaching a goal. Learning such state-action sequences from sparse reward raises the problem of credit-assignment: which actions out of a long sequence should be reinforced? One solution provided by reinforcement learning (RL) theory is the eligibility trace (ET); a decaying memory of the state-action history. Here we investigate behaviorally and neurally whether humans utilize an ET when learning a multi-step decision making task. We implemented three versions of a novel task using visual, acoustic, and spatial cues. Eleven subjects performed all three conditions while we recorded their pupil diameter. We considered model-based and model-free (with and without ET) algorithms to explain human learning. Using the Akaike Information Criterion (AIC) we find that model-free learning with ET explains the human behavior best in all three conditions. Cross-validation confirms this behavioral result. We then compare pupil dilation in early and late learning and observe differences that are consistent with an ET contribution. In particular, we find significant changes in pupil response to non-goal states after just a single reward in all three experimental conditions. In this research we introduce a novel paradigm to study the ET in human learning in a multi-step sequential decision making task. The analysis of the behavioral and pupil data provides evidence that humans utilize an eligibility trace to solve the credit-assignment problem when learning from sparse and delayed reward