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.

Storing and recalling spiking sequences is a general problem the brain needs to solve. It is, however, unclear what type of biologically plausible learning rule is suited to learn a wide class of spatiotemporal activity patterns in a robust way. Here we consider a recurrent network of stochastic spiking neurons composed of both visible and hidden neurons. We derive a generic learning rule that is matched to the neural dynamics by minimizing an upper bound on the Kullback-Leibler divergence from the target distribution to the model distribution. The derived learning rule is consistent with spike-timing dependent plasticity in that a presynaptic spike preceding a postsynaptic spike elicits potentiation while otherwise depression emerges. Furthermore, the learning rule for synapses that target visible neurons can be matched to the recently proposed voltage-triplet rule. The learning rule for synapses that target hidden neurons is modulated by a global factor, which shares properties with astrocytes and gives rise to testable predictions.

A B S T R A C TTraining deep neural networks with the error backpropagation algorithm is considered implausible from a biological perspective. Numerous recent publications suggest elaborate models for biologically plausible variants of deep learning, typically defining success as reaching around 98% test accuracy on the MNIST data set. Here, we investigate how far we can go on digit (MNIST) and object (CIFAR10) classification with biologically plausible, local learning rules in a network with one hidden layer and a single readout layer. The hidden layer weights are either fixed (random or random Gabor filters) or trained with unsupervised methods (Principal/Independent Component Analysis or Sparse Coding) that can be implemented by local learning rules. The readout layer is trained with a supervised, local learning rule. We first implement these models with rate neurons. This comparison reveals, first, that unsupervised learning does not lead to better performance than fixed random projections or Gabor filters for large hidden layers. Second, networks with localized receptive fields perform significantly better than networks with all-to-all connectivity and can reach backpropagation performance on MNIST. We then implement two of the networks -fixed, localized, random & random Gabor filters in the hidden layer -with spiking leaky integrate-and-fire neurons and spike timing dependent plasticity to train the readout layer. These spiking models achieve > 98.2% test accuracy on MNIST, which is close to the performance of rate networks with one hidden layer trained with backpropagation. The performance of our shallow network models is comparable to most current biologically plausible models of deep learning. Furthermore, our results with a shallow spiking network provide an important reference and suggest the use of datasets other than MNIST for testing the performance of future models of biologically plausible deep learning.

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.

Animals learn to make predictions, such as associating the sound of a bell with upcoming feeding or predicting a movement that a motor command is eliciting. How predictions are realized on the neuronal level and what plasticity rule underlies their learning is not well understood. Here we propose a biologically plausible synaptic plasticity rule to learn predictions on a single neuron level on a timescale of seconds. The learning rule allows a spiking two-compartment neuron to match its current firing rate to its own expected future discounted firing rate. For instance, if an originally neutral event is repeatedly followed by an event that elevates the firing rate of a neuron, the originally neutral event will eventually also elevate the neuron’s firing rate. The plasticity rule is a form of spike timing dependent plasticity in which a presynaptic spike followed by a postsynaptic spike leads to potentiation. Even if the plasticity window has a width of 20 milliseconds, associations on the time scale of seconds can be learned. We illustrate prospective coding with three examples: learning to predict a time varying input, learning to predict the next stimulus in a delayed paired-associate task and learning with a recurrent network to reproduce a temporally compressed version of a sequence. We discuss the potential role of the learning mechanism in classical trace conditioning. In the special case that the signal to be predicted encodes reward, the neuron learns to predict the discounted future reward and learning is closely related to the temporal difference learning algorithm TD(λ).

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Recent experiments revealed that the fruit fly Drosophila melanogaster has a dedicated mechanism for forgetting: blocking the G-protein Rac leads to slower and activating Rac to faster forgetting. This active form of forgetting lacks a satisfactory functional explanation. We investigated optimal decision making for an agent adapting to a stochastic environment where a stimulus may switch between being indicative of reward or punishment. Like Drosophila, an optimal agent shows forgetting with a rate that is linked to the time scale of changes in the environment. Moreover, to reduce the odds of missing future reward, an optimal agent may trade the risk of immediate pain for information gain and thus forget faster after aversive conditioning. A simple neuronal network reproduces these features. Our theory shows that forgetting in Drosophila appears as an optimal adaptive behavior in a changing environment. This is in line with the view that forgetting is adaptive rather than a consequence of limitations of the memory system.