Matched Short-Term Depression and Recovery Encodes Interspike Interval at a Central Synapse

Armando E Castillo,Sergio Rossoni,Jeremy E Niven

doi:10.1038/s41598-018-31996-0

Abstract

Reversible decreases in synaptic strength, known as short-term depression (STD), are widespread in neural circuits. Various computational roles have been attributed to STD but these tend to focus upon the initial depression rather than the subsequent recovery. We studied the role of STD and recovery at an excitatory synapse between the fast extensor tibiae (FETi) and flexor tibiae (flexor) motor neurons in the desert locust (Schistocerca gregaria) by making paired intracellular recordings in vivo. Over behaviorally relevant pre-synaptic spike frequencies, we found that this synapse undergoes matched frequency-dependent STD and recovery; higher frequency spikes that evoke stronger, faster STD also produce stronger, faster recovery. The precise matching of depression and recovery time constants at this synapse ensures that flexor excitatory post-synaptic potential (EPSP) amplitude encodes the presynaptic FETi interspike interval (ISI). Computational modelling shows that this precise matching enables the FETi-flexor synapse to linearly encode the ISI in the EPSP amplitude, a coding strategy that may be widespread in neural circuits.

Highlights

The short-term depression (STD) of synaptic strength has been proposed to perform a variety of computational roles in neural circuits, including low pass filtering of synaptic inputs[1,2,3], and reducing sensitivity to presynaptic activity[1]
The steady-state excitatory post-synaptic potential (EPSP) amplitude was significantly different among the frequencies we tested (F3,52 = 323.6, p < 0.001, N = 16; one-way ANOVA), demonstrating that STD is frequency-dependent at the fast extensor tibia motor neuron (FETi)-flexor synapse[6]
The dependence of EPSP amplitude upon interspike interval (ISI) duration allows the FETi-flexor synapse to encode spike timing over a range of intervals that occur during natural behavior in vivo

Summary

Introduction

The short-term depression (STD) of synaptic strength has been proposed to perform a variety of computational roles in neural circuits, including low pass filtering of synaptic inputs[1,2,3], and reducing sensitivity to presynaptic activity[1]. We recorded from a single presynaptic neuron, the fast extensor tibia motor neuron (FETi) (Figs 1C, S1A–D), and one of nine flexor tibiae motor neurons (flexors) in the metathoracic ganglion (Fig. 1D)[12] In this ganglion, FETi forms a monosynaptic connection with the flexors, which can each be characterized as slow, intermediate or fast depending upon their electrical activity and the movements of the tibia that they evoke (Fig. 1E)[13]. FETi forms a monosynaptic connection with the flexors, which can each be characterized as slow, intermediate or fast depending upon their electrical activity and the movements of the tibia that they evoke (Fig. 1E)[13] As their names imply, FETi and the flexors innervate the antagonistic extensor tibiae and flexor tibiae muscles that control extension and flexion of the hind tibia, respectively. Flexor EPSP amplitude responds rapidly to shifts in FETi activity, permitting these motor neurons to contribute to motor patterns underpinning a wide range of behaviours

Methods

Results

Conclusion