A functional spiking-neuron model of activity-silent working memory in humans based on calcium-mediated short-term synaptic plasticity

In this paper, we present a functional spiking-neuron model of human working memory (WM). This model combines neural firing for encoding of information with activity-silent maintenance. While it used to be widely assumed that information in WM is maintained through persistent recurrent activity, recent studies have shown that information can be maintained without persistent firing; instead, information can be stored in activity-silent states. A candidate mechanism underlying this type of storage is short-term synaptic plasticity (STSP), by which the strength of connections between neurons rapidly changes to encode new information. To demonstrate that STSP can lead to functional behavior, we integrated STSP by means of calcium-mediated synaptic facilitation in a large-scale spiking-neuron model and added a decision mechanism. The model was used to simulate a recent study that measured behavior and EEG activity of participants in three delayed-response tasks. In these tasks, one or two visual gratings had to be maintained in WM, and compared to subsequent probes. The original study demonstrated that WM contents and its priority status could be decoded from neural activity elicited by a task-irrelevant stimulus displayed during the activity-silent maintenance period. In support of our model, we show that it can perform these tasks, and that both its behavior as well as its neural representations are in agreement with the human data. We conclude that information in WM can be effectively maintained in activity-silent states by means of calcium-mediated STSP.Author SummaryMentally maintaining information for short periods of time in working memory is crucial for human adaptive behavior. It was recently shown that the human brain does not only store information through neural firing – as was widely believed – but also maintains information in activity-silent states. Here, we present a detailed neural model of how this could happen in our brain through short-term synaptic plasticity: rapidly adapting the connection strengths between neurons in response to incoming information. By reactivating the adapted network, the stored information can be read out later. We show that our model can perform three working memory tasks as accurately as human participants can, while using similar mental representations. We conclude that our model is a plausible and effective neural implementation of human working memory.