Network-timing-dependent plasticity.

Vincent Delattre,Eilif B Muller,Matthew Perich,Henry Markram,Daniel Keller

doi:10.3389/fncel.2015.00220

Vincent Delattre, Eilif B Muller + Show 3 more

Open Access

https://doi.org/10.3389/fncel.2015.00220

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Abstract

Bursts of activity in networks of neurons are thought to convey salient information and drive synaptic plasticity. Here we report that network bursts also exert a profound effect on Spike-Timing-Dependent Plasticity (STDP). In acute slices of juvenile rat somatosensory cortex we paired a network burst, which alone induced long-term depression (LTD), with STDP-induced long-term potentiation (LTP) and LTD. We observed that STDP-induced LTP was either unaffected, blocked or flipped into LTD by the network burst, and that STDP-induced LTD was either saturated or flipped into LTP, depending on the relative timing of the network burst with respect to spike coincidences of the STDP event. We hypothesized that network bursts flip STDP-induced LTP to LTD by depleting resources needed for LTP and therefore developed a resource-dependent STDP learning rule. In a model neural network under the influence of the proposed resource-dependent STDP rule, we found that excitatory synaptic coupling was homeostatically regulated to produce power law distributed burst amplitudes reflecting self-organized criticality, a state that ensures optimal information coding.

Highlights

Periods of synchronous neuronal firing, or bursts of action potentials (APs) in populations of neurons, are ubiquitous in the central nervous system
To gain insight into the proposed interaction of Spike-Timing-Dependent Plasticity (STDP) and network bursting activity, we investigated in vitro the effect of precisely timed network bursts on STDP at excitatory synaptic inputs to layer 5 pyramidal neurons where the STDP phenomenon was first reported (Markram et al, 1997)
We found that the bursts still flipped the long-term potentiation (LTP) into long-term depression (LTD) (Figure 3D; burst at T = –20 ms + PTX; open red circles; excitatory postsynaptic potential (EPSP) amp = –26 ± 14%, p = 0.18 against STDP+ and p = 0.38 against burst + STDP+, n = 5), indicating that inhibitory inputs do not play a significant role in burst-dependent

Summary

Introduction

Periods of synchronous neuronal firing, or bursts of action potentials (APs) in populations of neurons, are ubiquitous in the central nervous system. The pairing of STDP events with network bursts can influence the plasticity outcome by altering the timing relationship in the pre–post spike motif due to the additional spikes, and by changes in context due to the network burst (such as voltage, competition for resources, etc.) To separate the former effects from the latter, we performed burst-spike-substitution (BSS) experiments whereby the MEA burst was replaced with an excitatory postsynaptic potential (EPSP) paired with a simultaneous post-synaptic AP. We further hypothesize that the observed negative cooperativity could have an important role in the maintenance of the excitation–inhibition balance and of network criticality in the presence of on-going synaptic plasticity To evaluate this hypothesis, we employ simulations of networks of neurons incorporating an empirically constrained STDP rule (Morrison et al, 2007), and augment it with a resource depletion term implementing a shift of STDP outcomes from LTP to LTD when embedded in a network burst. The proposed resource-dependent interaction between network activity and STDP represents a novel mechanism for the homeostatic regulation of the network activity regime

Materials and Methods

Findings

Discussion