Abstract

Temporally precise sequences of neuronal spikes that span hundreds of milliseconds are observed in many brain areas, including songbird premotor nucleus, cat visual cortex, and primary motor cortex. Synfire chains—networks in which groups of neurons are connected via excitatory synapses into a unidirectional chain—are thought to underlie the generation of such sequences. It is unknown, however, how synfire chains can form in local neural circuits, especially for long chains. Here, we show through computer simulation that long synfire chains can develop through spike-time dependent synaptic plasticity and axon remodeling—the pruning of prolific weak connections that follows the emergence of a finite number of strong connections. The formation process begins with a random network. A subset of neurons, called training neurons, intermittently receive superthreshold external input. Gradually, a synfire chain emerges through a recruiting process, in which neurons within the network connect to the tail of the chain started by the training neurons. The model is robust to varying parameters, as well as natural events like neuronal turnover and massive lesions. Our model suggests that long synfire chain can form during the development through self-organization, and axon remodeling, ubiquitous in developing neural circuits, is essential in the process.

Highlights

  • Timed sequential firing of neurons has been observed in vivo in a number of brain areas

  • We aim to show that long synfire chains emerge in a network of spontaneously spiking neurons, through connectivity modifications driven by Hebbian synaptic plasticity and axon remodeling when a subset of them are activated intermittently by external inputs

  • A neuron contacts many postsynaptic targets with weak or silent synapses. Such exuberant connections make it possible for synchronously firing neuron groups, like the training neurons, to find new recruit neurons to add at the end of the existing chain

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Summary

Introduction

Timed sequential firing of neurons has been observed in vivo in a number of brain areas. Visual cortical neurons in anesthetized cats [2] and cortical motor neurons in behaving monkeys [3] exhibit spike sequences with precise timings spanning hundreds of milliseconds. Such sequences may serve as an infrastructure for learning temporally demanding tasks, such as well-timed motor actions and perceptual discriminations of temporal signals. Previous theoretical and experimental studies have shown that synfire chains are robust for spike sequence generation [10,11] They have been proposed as the neural mechanism that underlies the precise spike sequences observed in the zebra finch premotor neurons [12]

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