Abstract

Remembering the temporal order of a sequence of events is a task easily performed by humans in everyday life, but the underlying neuronal mechanisms are unclear. This problem is particularly intriguing as human behavior often proceeds on a time scale of seconds, which is in stark contrast to the much faster millisecond time-scale of neuronal processing in our brains. One long-held hypothesis in sequence learning suggests that a particular temporal fine-structure of neuronal activity - termed 'phase precession' - enables the compression of slow behavioral sequences down to the fast time scale of the induction of synaptic plasticity. Using mathematical analysis and computer simulations, we find that - for short enough synaptic learning windows - phase precession can improve temporal-order learning tremendously and that the asymmetric part of the synaptic learning window is essential for temporal-order learning. To test these predictions, we suggest experiments that selectively alter phase precession or the learning window and evaluate memory of temporal order.

Highlights

  • It is a pivotal quality for animals to be able to store and recall the order of events (“temporal-order learning”, 1–3) but there is only little work on the neural mechanisms generating asymmetric memory associations across behavioral time intervals [4]

  • The faster time scale is given by the temporal properties of the induction of synaptic plasticity [6, 7] — and spike-timing dependent plasticity (STDP) is a common form of synaptic plasticity that depends on the millisecond timing and temporal order of presynaptic and postsynaptic spiking

  • We show that phase precession facilitates the learning of the temporal order of behavioral sequences for asymmetric learning windows that are shorter than a theta cycle

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Summary

Introduction

It is a pivotal quality for animals to be able to store and recall the order of events (“temporal-order learning”, 1–3) but there is only little work on the neural mechanisms generating asymmetric memory associations across behavioral time intervals [4]. Phase precession allows for a temporal compression of a sequence of behavioral events from the time scale of seconds down to milliseconds (Fig. 1;12–14), which matches the widths of generic STDP learning windows [15,16,17,18]. This putative advantage of phase precession for temporal-order learning, has not yet been quantified. We provide a mechanistic description of associative chaining models [19] and extend these models to explain how to store serial order

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