Abstract

Learning and memory formation are processes which are still not fully understood. It is widely believed that synaptic plasticity is the most important neural substrate for both. However, it has been observed that large-scale theta band oscillations in the mammalian brain are beneficial for learning, and it is not clear if and how this is linked to synaptic plasticity. Also, the underlying dynamics of synaptic plasticity itself have not been completely uncovered yet, especially for non-linear interactions between multiple spikes. Here, we present a new and simple dynamical model of synaptic plasticity. It incorporates novel contributions to synaptic plasticity including adaptation processes. We test its ability to reproduce non-linear effects on four different data sets of complex spike patterns, and show that the model can be tuned to reproduce the observed synaptic changes in great detail. When subjected to periodically varying firing rates, already linear pair based spike timing dependent plasticity (STDP) predicts a specific susceptibility of synaptic plasticity to pre- and postsynaptic firing rate oscillations in the theta-band. Our model retains this band-pass property, while for high firing rates in the non-linear regime it modifies the specific phase relation required for depression and potentiation. For realistic parameters, maximal synaptic potentiation occurs when the postsynaptic is trailing the presynaptic activity slightly. Anti-phase oscillations tend to depress it. Our results are well in line with experimental findings, providing a straightforward and mechanistic explanation for the importance of theta oscillations for learning.

Highlights

  • Synaptic plasticity likely is the key neural substrate underlying learning and memory in the brain

  • Ideas on the problem of synaptic plasticity posited that positive correlations between neuronal activities are the signal for the synapse to potentiate; later experiments showed that the relevant signal is not just the average correlation of activity, but rather the precise temporal order of single spikes at the pre- and postsynaptic neuron (Markram et al, 1997; Bi and Poo, 1998; Zhang et al, 1998; Feldman, 2000)

  • We found that the CD model has unique properties which tie in with experimental findings on the connection of theta oscillations and memory formation, providing a mechanistic link between synaptic plasticity and the beneficial nature of theta-band oscillations for learning

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Summary

Introduction

Synaptic plasticity likely is the key neural substrate underlying learning and memory in the brain. Ideas on the problem of synaptic plasticity posited that positive correlations between neuronal activities are the signal for the synapse to potentiate (see e.g., review by Markram et al, 2011); later experiments showed that the relevant signal is not just the average correlation of activity, but rather the precise temporal order of single spikes at the pre- and postsynaptic neuron (Markram et al, 1997; Bi and Poo, 1998; Zhang et al, 1998; Feldman, 2000). Other experiments show that contrary to expectation a single pre-post pair fails to potentiate the synapse, but a pre-post-post triplet leads to strong long term potentiation (LTP) (Sjöström et al, 2001; Nevian and Sakmann, 2006; Wittenberg and Wang, 2006) These findings highlight the need for any accurate model of STDP to include non-linearities. An attenuated synaptic response to repeated high frequency spiking [Short term depression,

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