Ultrastructural analysis of dendritic spine necks reveals a continuum of spine morphologies

Abstract

Dendritic spines are membranous protrusions, with a bulbous head connected to the dendrite by a thin neck, and receive essentially all excitatory inputs in most mammalian neurons. Spines have a wide variety of morphologies that likely have a significant effect on their biochemical and electrical properties. The question of whether spines belong to distinct morphological or functional subtypes or constitute a continuum is still open. To discern this, it is important to measure spine necks objectively. Recent advances in electron microscopy enable automatic reconstructions of 3D spines with nanometer precision. Analyzing ultrastructural reconstructions from mouse neocortical neurons with computer vision algorithms, we demonstrate that the vast majority of spines can be rigorously separated into head and neck components. Analysis of the head and neck morphologies reveals a continuous distribution of parameters. The spine neck diameter, but not the neck length, was correlated with the head volume. Spines with larger head volumes often had a spine apparatus and pairs of spines in a post-synaptic cell contacted by the same axon had similar head volumes. Our data are consistent with a lack of morphological categories of spines and indicate that the morphologies of the spine neck and head are independently regulated. These results have repercussions for our understanding of the function of dendritic spines in neuronal circuits.