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.

The ongoing motor output of the brain depends on its remarkable ability to rapidly transform and fuse a variety of sensory streams in real-time. The brain processes these data using networks of neurons that communicate by asynchronous spikes, a technology that is dramatically different from conventional electronic systems. We report here a step towards constructing electronic systems with analogous performance to the brain. Our VLSI spiking neural network combines in real-time three distinct sources of input data; each is place-encoded on an individual neuronal population that expresses soft Winner-Take-All dynamics. These arrays are combined according to a user-specified function that is embedded in the reciprocal connections between the soft Winner-Take-All populations and an intermediate shared population. The overall network is able to perform function approximation (missing data can be inferred from the available streams) and cue integration (when all input streams are present they enhance one another synergistically). The network performs these tasks with about 80% and 90% reliability, respectively. Our results suggest that with further technical improvement, it may be possible to implement more complex probabilistic models such as Bayesian networks in neuromorphic electronic systems. Abstract-The ongoing motor output of the brain depends on its remarkable ability to rapidly transform and fuse a variety of sensory streams in real-time. The brain processes these data using networks of neurons that communicate by asynchronous spikes, a technology that is dramatically different from conventional electronic systems. We report here a step towards constructing electronic systems with analogous performance to the brain. Our VLSI spiking neural network combines in real-time three distinct sources of input data; each is place-encoded on an individual neuronal population that expresses soft Winner-Take-All dynamics. These arrays are combined according to a user-specified function that is embedded in the reciprocal connections between the soft Winner-Take-All populations and an intermediate shared population. The overall network is able to perform function approximation (missing data can be inferred from the available streams) and cue integration (when all input streams are present they enhance one another synergistically). The network performs these tasks with about 80% and 90% reliability, respectively. Our results suggest that with further technical improvement, it may be possible to implement more complex probabilistic models such as Bayesian networks in neuromorphic electronic systems.

Abstract-The brain combines and integrates multiple cues to take coherent, context-dependent action using distributed, eventbased computational primitives. Computational models that use these principles in software simulations of recurrently coupled spiking neural networks have been demonstrated in the past, but their implementation in hybrid analog/digital Very Large Scale Integration (VLSI) spiking neural networks remains challenging. Here, we demonstrate a distributed spiking neural network architecture comprising multiple neuromorphic VLSI chips able to reproduce these types of cue combination and integration operations. This is achieved by encoding cues as population activities of input nodes in a network of recurrently coupled VLSI Integrate-and-Fire (I&F) neurons. The value of the cue is place-encoded, while its uncertainty is represented by the width of the population activity profile. Relationships among different cues are specified through bidirectional connectivity matrices, shared between the individual input node populations and an intermediate node population. The resulting network dynamics bidirectionally relate not only the values of three variables according to a specified relation, but also their uncertainties. When cues on two populations are specified, the standard deviation of the activity in the unspecified population varies approximately linearly with the widths of the two input cues, and has less than 6% error in position compared to the value specified by the inputs. The results suggest a mechanism for recurrently relating cues such that missing information can both be recovered and assigned a level of certainty.