Abstract

Short-term synaptic plasticity (STP) is an important mechanism for modifying neural circuits during computation. Although STP is much studied, its role in the processing of complex natural spike patterns is unknown. Here we analyze the responses of excitatory and inhibitory hippocampal synapses to natural spike trains at near-physiological temperatures. Our results show that excitatory and inhibitory synapses express complementary sets of STP components that selectively change synaptic strength during epochs of high-frequency discharge associated with hippocampal place fields. In both types of synapses, synaptic strength rapidly alternates between a near-constant level during low activity and another near-constant, but elevated (for excitatory synapses) or reduced (for inhibitory synapses) level during high-frequency epochs. These history-dependent changes in synaptic strength are largely independent of the particular temporal pattern within the discharges, and occur concomitantly in the two types of synapses. When excitatory and feed-forward inhibitory synapses are co-activated within the hippocampal feed-forward circuit unit, the net effect of their complementary STP is an additional increase in the gain of excitatory synapses during high-frequency discharges via selective disinhibition. Thus, excitatory and feed-forward inhibitory hippocampal synapses in vitro act synergistically as an adaptive filter that operates in a switch-like manner and is selective for high-frequency epochs.

Highlights

  • Synapses, commonly considered as computational units of the brain, process information encoded in the spike sequences via a dynamic, history-dependent modulation of synaptic transmission, known as short-term plasticity (STP) [1,2]

  • We find that excitatory and inhibitory synapses express conserved and complementary sets of STP components that are selective for the epochs of high-frequency discharge associated with hippocampal place fields

  • After correcting synaptic responses for contributions from facilitation and augmentation [45], we found that, at 33–34 8C, excitatory postsynaptic current (EPSC) depressed during the train at least as much as inhibitory postsynaptic current (IPSC) (0.35 6 0.04 vs. 0.43 6 0.04 at 250 ms after the train, n 1⁄4 9 and 5, respectively) (Figure 5E)

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Summary

Introduction

Commonly considered as computational units of the brain, process information encoded in the spike sequences via a dynamic, history-dependent modulation of synaptic transmission, known as short-term plasticity (STP) [1,2]. Both excitatory and inhibitory synapses express various forms of STP—facilitation, depression, or some mixture of both, depending on the particular type of synapse [3,4,5], the identity of pre- and/or postsynaptic cells [6,7,8,9,10], and temporal characteristics of the electrical input [11,12,13,14].

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