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

A Reinforcement Learning Framework for Spiking Networks with Dynamic Synapses

An integration of both the Hebbian-based and reinforcement learning (RL) rules is presented for dynamic synapses. The proposed framework permits the Hebbian rule to update the hidden synaptic model parameters regulating the synaptic response rather than the synaptic weights. This is performed using both the value and the sign of the temporal difference in the reward signal after each trial. Applying this framework, a spiking network with spike-timing-dependent synapses is tested to learn the exclusive-OR computation on a temporally coded basis. Reward values are calculated with the distance between the output spike train of the network and a reference target one. Results show that the network is able to capture the required dynamics and that the proposed framework can reveal indeed an integrated version of Hebbian and RL. The proposed framework is tractable and less computationally expensive. The framework is applicable to a wide class of synaptic models and is not restricted to the used neural representation. This generality, along with the reported results, supports adopting the introduced approach to benefit from the biologically plausible synaptic models in a wide range of intuitive signal processing

Fast and robust learning by reinforcement signals: explorations in the insect brain

We propose a model for pattern recognition in the insect brain. Departing from a well-known body of knowledge about the insect brain, we investigate which of the potentially present features may be useful to learn input patterns rapidly and in a stable manner. The plasticity underlying pattern recognition is situated in the insect mushroom bodies and requires an error signal to associate the stimulus with a proper response. As a proof of concept, we used our model insect brain to classify the well-known MNIST database of handwritten digits, a popular benchmark for classifiers. We show that the structural organization of the insect brain appears to be suitable for both fast learning of new stimuli and reasonable performance in stationary conditions. Furthermore, it is extremely robust to damage to the brain structures involved in sensory processing. Finally, we suggest that spatiotemporal dynamics can improve the level of confidence in a classification decision. The proposed approach allows testing the effect of hypothesized mechanisms rather than speculating on their benefit for system performance or confidence in its responses

Short-term plasticity as cause-effect hypothesis testing in distal reward learning

Asynchrony, overlaps and delays in sensory-motor signals introduce ambiguity as to which stimuli, actions, and rewards are causally related. Only the repetition of reward episodes helps distinguish true cause-effect relationships from coincidental occurrences. In the model proposed here, a novel plasticity rule employs short and long-term changes to evaluate hypotheses on cause-effect relationships. Transient weights represent hypotheses that are consolidated in long-term memory only when they consistently predict or cause future rewards. The main objective of the model is to preserve existing network topologies when learning with ambiguous information flows. Learning is also improved by biasing the exploration of the stimulus-response space towards actions that in the past occurred before rewards. The model indicates under which conditions beliefs can be consolidated in long-term memory, it suggests a solution to the plasticity-stability dilemma, and proposes an interpretation of the role of short-term plasticity.Comment: Biological Cybernetics, September 201

Neuromodulated synaptic plasticity on the SpiNNaker neuromorphic system

SpiNNaker is a digital neuromorphic architecture, designed specifically for the low power simulation of large-scale spiking neural networks at speeds close to biological real-time. Unlike other neuromorphic systems, SpiNNaker allows users to develop their own neuron and synapse models as well as specify arbitrary connectivity. As a result SpiNNaker has proved to be a powerful tool for studying different neuron models as well as synaptic plasticity—believed to be one of the main mechanisms behind learning and memory in the brain. A number of Spike-Timing-Dependent-Plasticity(STDP) rules have already been implemented on SpiNNaker and have been shown to be capable of solving various learning tasks in real-time. However, while STDP is an important biological theory of learning, it is a form of Hebbian or unsupervised learning and therefore does not explain behaviors that depend on feedback from the environment. Instead, learning rules based on neuromodulated STDP (three-factor learning rules) have been shown to be capable of solving reinforcement learning tasks in a biologically plausible manner. In this paper we demonstrate for the first time how a model of three-factor STDP, with the third-factor representing spikes from dopaminergic neurons, can be implemented on the SpiNNaker neuromorphic system. Using this learning rule we first show how reward and punishment signals can be delivered to a single synapse before going on to demonstrate it in a larger network which solves the credit assignment problem in a Pavlovian conditioning experiment. Because of its extra complexity, we find that our three-factor learning rule requires approximately 2× as much processing time as the existing SpiNNaker STDP learning rules. However, we show that it is still possible to run our Pavlovian conditioning model with up to 1 × 104 neurons in real-time, opening up new research opportunities for modeling behavioral learning on SpiNNaker

Phenomenological models of synaptic plasticity based on spike timing

Synaptic plasticity is considered to be the biological substrate of learning and memory. In this document we review phenomenological models of short-term and long-term synaptic plasticity, in particular spike-timing dependent plasticity (STDP). The aim of the document is to provide a framework for classifying and evaluating different models of plasticity. We focus on phenomenological synaptic models that are compatible with integrate-and-fire type neuron models where each neuron is described by a small number of variables. This implies that synaptic update rules for short-term or long-term plasticity can only depend on spike timing and, potentially, on membrane potential, as well as on the value of the synaptic weight, or on low-pass filtered (temporally averaged) versions of the above variables. We examine the ability of the models to account for experimental data and to fulfill expectations derived from theoretical considerations. We further discuss their relations to teacher-based rules (supervised learning) and reward-based rules (reinforcement learning). All models discussed in this paper are suitable for large-scale network simulation

Phenomenological models of synaptic plasticity based on spike timing

Synaptic plasticity is considered to be the biological substrate of learning and memory. In this document we review phenomenological models of short-term and long-term synaptic plasticity, in particular spike-timing dependent plasticity (STDP). The aim of the document is to provide a framework for classifying and evaluating different models of plasticity. We focus on phenomenological synaptic models that are compatible with integrate-and-fire type neuron models where each neuron is described by a small number of variables. This implies that synaptic update rules for short-term or long-term plasticity can only depend on spike timing and, potentially, on membrane potential, as well as on the value of the synaptic weight, or on low-pass filtered (temporally averaged) versions of the above variables. We examine the ability of the models to account for experimental data and to fulfill expectations derived from theoretical considerations. We further discuss their relations to teacher-based rules (supervised learning) and reward-based rules (reinforcement learning). All models discussed in this paper are suitable for large-scale network simulations

Spike-Based Reinforcement Learning in Continuous State and Action Space: When Policy Gradient Methods Fail

Changes of synaptic connections between neurons are thought to be the physiological basis of learning. These changes can be gated by neuromodulators that encode the presence of reward. We study a family of reward-modulated synaptic learning rules for spiking neurons on a learning task in continuous space inspired by the Morris Water maze. The synaptic update rule modifies the release probability of synaptic transmission and depends on the timing of presynaptic spike arrival, postsynaptic action potentials, as well as the membrane potential of the postsynaptic neuron. The family of learning rules includes an optimal rule derived from policy gradient methods as well as reward modulated Hebbian learning. The synaptic update rule is implemented in a population of spiking neurons using a network architecture that combines feedforward input with lateral connections. Actions are represented by a population of hypothetical action cells with strong mexican-hat connectivity and are read out at theta frequency. We show that in this architecture, a standard policy gradient rule fails to solve the Morris watermaze task, whereas a variant with a Hebbian bias can learn the task within 20 trials, consistent with experiments. This result does not depend on implementation details such as the size of the neuronal populations. Our theoretical approach shows how learning new behaviors can be linked to reward-modulated plasticity at the level of single synapses and makes predictions about the voltage and spike-timing dependence of synaptic plasticity and the influence of neuromodulators such as dopamine. It is an important step towards connecting formal theories of reinforcement learning with neuronal and synaptic properties