Short-Term Synaptic Plasticity at Interneuronal Synapses Could Sculpt Rhythmic Motor Patterns.

Yan Jia,David Parker

doi:10.3389/fncir.2016.00004

Abstract

The output of a neuronal network depends on the organization and functional properties of its component cells and synapses. While the characterization of synaptic properties has lagged cellular analyses, a potentially important aspect in rhythmically active networks is how network synapses affect, and are in turn affected by, network activity. This could lead to a potential circular interaction where short-term activity-dependent synaptic plasticity is both influenced by and influences the network output. The analysis of synaptic plasticity in the lamprey locomotor network was extended here to characterize the short-term plasticity of connections between network interneurons and to try and address its potential network role. Paired recordings from identified interneurons in quiescent networks showed synapse-specific synaptic properties and plasticity that supported the presence of two hemisegmental groups that could influence bursting: depression in an excitatory interneuron group, and facilitation in an inhibitory feedback circuit. The influence of activity-dependent synaptic plasticity on network activity was investigated experimentally by changing Ringer Ca2+ levels, and in a simple computer model. A potential caveat of the experimental analyses was that changes in Ringer Ca2+ (and compensatory adjustments in Mg2+ in some cases) could alter several other cellular and synaptic properties. Several of these properties were tested, and while there was some variability, these were not usually significantly affected by the Ringer changes. The experimental analyses suggested that depression of excitatory inputs had the strongest influence on the patterning of network activity. The simulation supported a role for this effect, and also suggested that the inhibitory facilitating group could modulate the influence of the excitatory synaptic depression. Short-term activity-dependent synaptic plasticity has not generally been considered in spinal cord models. These results provide further evidence for short-term plasticity between locomotor network interneurons. As this plasticity could influence the patterning of the network output it should be considered as a potential functional component of spinal cord networks.

Highlights

IntroductionIn the original formulation of the locomotor network scheme (see for example Grillner et al, 1995), each hemisegment has excitatory interneurons (EIN) that connect to motor neurons, the large crossed caudal (CC) inhibitory interneurons, and the large inhibitory lateral interneurons (LIN; Buchanan et al, 1989); the CC interneurons inhibit contralateral motor neurons, LINs, and other CC interneurons (Buchanan, 1982), as well as the EINs; and the LINs inhibit the CC interneurons and motor neurons (Rovainen, 1974; Buchanan, 1982)
The short-term activity-dependent plasticity of individual synapses has been studied extensively (Zucker and Regehr, 2002), its role within neuronal networks remains difficult to address
In the original formulation of the locomotor network scheme, each hemisegment has excitatory interneurons (EIN) that connect to motor neurons, the large crossed caudal (CC) inhibitory interneurons, and the large inhibitory lateral interneurons (LIN; Buchanan et al, 1989); the CC interneurons inhibit contralateral motor neurons, LINs, and other CC interneurons (Buchanan, 1982), as well as the EINs; and the LINs inhibit the CC interneurons and motor neurons (Rovainen, 1974; Buchanan, 1982)

Summary

Introduction

In the original formulation of the locomotor network scheme (see for example Grillner et al, 1995), each hemisegment has excitatory interneurons (EIN) that connect to motor neurons, the large crossed caudal (CC) inhibitory interneurons, and the large inhibitory lateral interneurons (LIN; Buchanan et al, 1989); the CC interneurons inhibit contralateral motor neurons, LINs, and other CC interneurons (Buchanan, 1982), as well as the EINs; and the LINs inhibit the CC interneurons and motor neurons (Rovainen, 1974; Buchanan, 1982) This network, and its modification (Grillner, 2003) after problems with the classical network scheme were highlighted (Parker, 2000), are claimed by Grillner to offer a fully characterized network organization. The SiINs and ScINs have been examined, the connectivity of these cells, their functional properties, and their role in the network still remains poorly understood (Parker, 2006, 2010)

Methods

Results

Conclusion