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

Matthijs Pals,Jelmer P Borst,Elkan G Akyürek,Terrence C Stewart,Abigail Morrison

doi:10.1371/journal.pcbi.1007936

Matthijs Pals, Jelmer P Borst + Show 3 more

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https://doi.org/10.1371/journal.pcbi.1007936

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Abstract

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.

Highlights

The ability to temporarily hold information in working memory (WM) is a crucial part of dayto-day life: it is what allows us to remember someone’s name at a cocktail party, what ingredients to buy at the supermarket for dinner, and which platform we need to go to when changing trains [1,2]
The maintenance of information in WM is often studied by means of a delayedresponse task, in which a briefly presented memory item is followed by a delay period [3,4]
Because calcium is much slower to return to its baseline levels than the resources, the synaptic connection is facilitated in the long-term, for about 1.5 seconds

Summary

Introduction

The ability to temporarily hold information in working memory (WM) is a crucial part of dayto-day life: it is what allows us to remember someone’s name at a cocktail party, what ingredients to buy at the supermarket for dinner, and which platform we need to go to when changing trains [1,2]. The maintenance of information in WM is often studied by means of a delayedresponse task, in which a briefly presented memory item is followed by a delay period [3,4]. Neural spiking is certainly important for WM, it was recently shown that spiking activity during delay periods can be intermittent or even absent [7,8,9,10,11]. This suggests that information may be stored instead using activity-silent mechanisms, for instance through transient connectivity patterns in the brain [2,12,13]. The spiking activity observed previously might reflect the initial phase necessary to initialize new synaptic weights, active maintenance of the focus of attention [14,15,16,17], or the read-out of information from working memory [13,18]

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