Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies

Abstract

Dendritic spines are critical elements of cortical circuits, since they establish most excitatory synapses. Recent studies have reported correlations between morphological and functional parameters of spines. Specifically, the spine head volume is correlated with the area of the postsynaptic density (PSD), the number of postsynaptic receptors and the ready-releasable pool of transmitter, whereas the length of the spine neck is proportional to the degree of biochemical and electrical isolation of the spine from its parent dendrite. Therefore, the morphology of a spine could determine its synaptic strength and learning rules.To better understand the natural variability of neocortical spine morphologies, we used a combination of gold-toned Golgi impregnations and serial thin-section electron microscopy and performed three-dimensional reconstructions of spines from layer 2/3 pyramidal cells from mouse visual cortex. We characterized the structure and synaptic features of 144 completed reconstructed spines, and analyzed their morphologies according to their positions. For all morphological parameters analyzed, spines exhibited a continuum of variability, without clearly distinguishable subtypes of spines or clear dependence of their morphologies on their distance to the soma. On average, the spine head volume was correlated strongly with PSD area and weakly with neck diameter, but not with neck length. The large morphological diversity suggests an equally large variability of synaptic strength and learning rules.

Dendritic Spine Dynamics Regulate the Long-Term Stability of Synaptic Plasticity

“…They are typically continuous, unimodal, and have a peak at a nonzero strength and a long tail at high strengths. Although some electrophysiological and light microscopy techniques have noise amplitudes that make them likely to underestimate the prevalence of weak synapses, we note that the qualitative feature of a unimodal distribution with nonzero peak is also reproduced by studies employing electron microscopy, where image resolution is beyond that necessary to unambiguously measure synapses of all size (Harris and Stevens, 1989;Schikorski and Stevens, 1997;Arellano et al, 2007;Mishchenko et al, 2010).…”

Spine neck plasticity regulates compartmentalization of synapses

“…Electron microscopy studies have provided exquisitely detailed and quantitative analyses of spine morphology in fixed samples 24,38,39 , but a comparable analysis in live tissue has been lacking. Our STED images reveal a high degree of heterogeneity of spine sizes and morphologies, which agrees well with the previous electron microscopy work, but argues against morphological categorization schemes commonly used in the light microscopic literature [40][41][42] .…”

Multiplicative Dynamics Underlie the Emergence of the Log-Normal Distribution of Spine Sizes in the Neocortex In Vivo

“…Therefore, these efficacies reflect the mental history of the animal. Intriguingly, previous studies have shown that the distribution of connection strengths in the cortex is skewed (Feldmeyer et al, 2002;Arellano et al, 2007). Some studies approximated this distribution using a log-normal function (Song et al, 2005;Sarid et al, 2007).…”

“…There is substantial evidence that the size of a spine provides information about the efficacy of the synapse that resides on it: the volume of a spine is proportional to (1) the number of vesicles in the presynaptic terminal (Harris and Stevens, 1989); (2) the area of the postsynaptic density (Harris and Stevens, 1989;Knott et al, 2006;Arellano et al, 2007;Katz et al, 2009); (3) the number of postsynaptic AMPA receptors (Katz et al, 2009); and (4) the amplitude of the EPSC measured in the postsynaptic neuron following uncaging of glutamate near the spine (Matsuzaki et al, 2001). Furthermore, long-term potentiation of synapses is associated with an increase in the volume of spines (Matsuzaki et al, 2004;Kopec et al, 2006).…”