Electrical behaviour of dendritic spines as revealed by voltage imaging.

Marko A Popovic,Balazs Rozsa,Dejan Zecevic,Nicholas Carnevale

doi:10.1038/ncomms9436

Marko A Popovic, Balazs Rozsa + Show 2 more

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https://doi.org/10.1038/ncomms9436

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Abstract

Thousands of dendritic spines on individual neurons process information and mediate plasticity by generating electrical input signals using a sophisticated assembly of transmitter receptors and voltage-sensitive ion channel molecules. Our understanding, however, of the electrical behaviour of spines is limited because it has not been possible to record input signals from these structures with adequate sensitivity and spatiotemporal resolution. Current interpretation of indirect data and speculations based on theoretical considerations are inconclusive. Here we use an electrochromic voltage-sensitive dye which acts as a transmembrane optical voltmeter with a linear scale to directly monitor electrical signals from individual spines on thin basal dendrites. The results show that synapses on these spines are not electrically isolated by the spine neck to a significant extent. Electrically, they behave as if they are located directly on dendrites.

Highlights

Thousands of dendritic spines on individual neurons process information and mediate plasticity by generating electrical input signals using a sophisticated assembly of transmitter receptors and voltage-sensitive ion channel molecules
An image of a cortical layer 5 pyramidal neuron situated in the superficial layer of the slice (o30 mm from the surface) and labelled with the voltage-sensitive dye was projected onto a charge-coupled device camera (CCD) for voltage imaging at high magnification so that individual spines could be clearly resolved (Fig. 1b)
We selected spines that were isolated from their neighbours both in x–y and in z dimension; the selection was biased against spines with small heads because these were characterized with poor signal-to-noise ratio

Summary

Introduction

Thousands of dendritic spines on individual neurons process information and mediate plasticity by generating electrical input signals using a sophisticated assembly of transmitter receptors and voltage-sensitive ion channel molecules. Spines are small (B1 mm) membrane protrusions from dendrites which receive most of the excitatory synaptic inputs in the mammalian brain They are of critical importance because they utilize a complex assembly of transmitter receptors and voltage-sensitive ion channel molecules[1] to process electrical input signals and to mediate synaptic plasticity that may underlie learning and memory[2]. Obtaining direct evidence on these variables requires a method for monitoring subthreshold membrane potential responses simultaneously from the spine head and the parent dendrite as well as a technique for a selective activation of individual excitatory synapses on the spine head. We used an advanced version of electrochromic voltage-sensitive dye technique[14] which allowed us to directly measure subthreshold excitatory postsynaptic potential (EPSP) signals from individual spines and quantify electrical resistance of the spine neck. The optical approach described here lights the way to future studies of how particular combinations of transmitter receptors and voltage-sensitive ion channels in different spines[15] act in concert to shape the integration of chemical input signals at the site of origin

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