Dendritic Voltage Recordings Explain Paradoxical Synaptic Plasticity: A Modeling Study.

Claire Meissner-Bernard,Wulfram Gerstner,Laureline Logiaco,Matthias Chinyen Tsai

doi:10.3389/fnsyn.2020.585539

Abstract

Experiments have shown that the same stimulation pattern that causes Long-Term Potentiation in proximal synapses, will induce Long-Term Depression in distal ones. In order to understand these, and other, surprising observations we use a phenomenological model of Hebbian plasticity at the location of the synapse. Our model describes the Hebbian condition of joint activity of pre- and postsynaptic neurons in a compact form as the interaction of the glutamate trace left by a presynaptic spike with the time course of the postsynaptic voltage. Instead of simulating the voltage, we test the model using experimentally recorded dendritic voltage traces in hippocampus and neocortex. We find that the time course of the voltage in the neighborhood of a stimulated synapse is a reliable predictor of whether a stimulated synapse undergoes potentiation, depression, or no change. Our computational model can explain the existence of different -at first glance seemingly paradoxical- outcomes of synaptic potentiation and depression experiments depending on the dendritic location of the synapse and the frequency or timing of the stimulation.

Highlights

How are memories encoded in the brain? In 1949, Donald Hebb postulated that a synapse connecting two neurons strengthens if both neurons are active together (Hebb, 1949)
We show that the time-course of the postsynaptic voltage in the neighborhood of the synapse, in combination with presynaptic signaling, is a reliable predictor of synaptic plasticity and is sufficient to explain the outcome of the experiments
Rather our philosophy is that the voltage time course, if experimentally available, is a very good indicator of whether or not synaptic changes are induced in those synapses that have been presynaptically stimulated

Summary

Introduction

How are memories encoded in the brain? In 1949, Donald Hebb postulated that a synapse connecting two neurons strengthens if both neurons are active together (Hebb, 1949). The critical postsynaptic signal for plasticity induction might be related to voltage (Artola et al, 1990), calcium (Cormier et al, 2001), or backpropagating action potentials (Markram et al, 1997b). If changes in subthreshold voltage or calcium concentration are the critical signals on the postsynaptic side, plasticity does not require the postsynaptic neuron to fire a somatic spike. If backpropagating action potentials are critical, synaptic plasticity outcomes can be completely described by the relative timing of pre- and postsynaptic spikes in the form of a Spike-Timing Dependent Plasticity rule (STDP rule, Abbott and Nelson, 2000). A first, and fundamental, challenge for all STDP models is the existence of subthreshold plasticity in the absence of somatic spikes

Results

Discussion

Conclusion