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      Ultrastructure of Dendritic Spines: Correlation Between Synaptic and Spine Morphologies

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          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.

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          Most cited references51

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          Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.

          An activity-dependent form of synaptic plasticity underlies the fine tuning of connections in the developing primary visual cortex of mammals such as the cat and monkey. Studies of the effects of manipulations of visual experience during a critical period have demonstrated that a correlation-based competitive process governs this plasticity. The cellular mechanisms underlying this competition, however, are poorly understood. Transgenic and gene-targeting technologies have led to the development of a new category of reagents that have the potential to help answer questions of cellular mechanism, provided that the questions can be studied in a mouse model. The current study attempts to characterize a developmental plasticity in the mouse primary visual cortex and to demonstrate its relevance to that found in higher mammals. We found that 4 d of monocular lid suture at postnatal day 28 (P28) induced a maximal loss of responsiveness of cortical neurons to the deprived eye. These ocular dominance shifts occurred during a well-defined critical period, between P19 and P32. Furthermore, binocular deprivation during this critical period did not decrease visual cortical responses, and alternating monocular deprivation resulted in a decrease in the number of binocularly responsive neurons. Finally, a laminar analysis demonstrated plasticity of both geniculocortical and intracortical connections. These results demonstrate that an activity-dependent, competitive form of synaptic plasticity that obeys correlation-based rules operates in the developing primary visual cortex of the mouse.
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            Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells.

            The integrative properties of neurons depend strongly on the number, proportions and distribution of excitatory and inhibitory synaptic inputs they receive. In this study the three-dimensional geometry of dendritic trees and the density of symmetrical and asymmetrical synapses on different cellular compartments of rat hippocampal CA1 area pyramidal cells was measured to calculate the total number and distribution of excitatory and inhibitory inputs on a single cell.A single pyramidal cell has approximately 12,000 microm dendrites and receives around 30,000 excitatory and 1700 inhibitory inputs, of which 40 % are concentrated in the perisomatic region and 20 % on dendrites in the stratum lacunosum-moleculare. The pre- and post-synaptic features suggest that CA1 pyramidal cell dendrites are heterogeneous. Strata radiatum and oriens dendrites are similar and differ from stratum lacunosum-moleculare dendrites. Proximal apical and basal strata radiatum and oriens dendrites are spine-free or sparsely spiny. Distal strata radiatum and oriens dendrites (forming 68.5 % of the pyramidal cells' dendritic tree) are densely spiny; their excitatory inputs terminate exclusively on dendritic spines, while inhibitory inputs target only dendritic shafts. The proportion of inhibitory inputs on distal spiny strata radiatum and oriens dendrites is low ( approximately 3 %). In contrast, proximal dendritic segments receive mostly (70-100 %) inhibitory inputs. Only inhibitory inputs innervate the somata (77-103 per cell) and axon initial segments. Dendrites in the stratum lacunosum-moleculare possess moderate to small amounts of spines. Excitatory synapses on stratum lacunosum-moleculare dendrites are larger than the synapses in other layers, are frequently perforated ( approximately 40 %) and can be located on dendritic shafts. Inhibitory inputs, whose percentage is relatively high ( approximately 14-17 %), also terminate on dendritic spines. Our results indicate that: (i) the highly convergent excitation arriving onto the distal dendrites of pyramidal cells is primarily controlled by proximally located inhibition; (ii) the organization of excitatory and inhibitory inputs in layers receiving Schaffer collateral input (radiatum/oriens) versus perforant path input (lacunosum-moleculare) is significantly different.
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              Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function.

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                Author and article information

                Journal
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Research Foundation
                1662-4548
                1662-453X
                01 September 2007
                15 October 2007
                November 2007
                : 1
                : 1
                : 131-143
                Affiliations
                [1] 1Instituto Cajal, Madrid Spain
                [2] 2HHMI, Department of Biological Sciences, Columbia University, New York USA
                Author notes

                Review Editors: Gordon Shepherd, Department of Neurobiology, Yale University School of Medicine, USA; Kristen Harris, Center for Learning and Memory, The University of Texas at Austin, USA

                *Correspondence: Javier DeFelipe and Yuste, Instituto Cajal (CSIC), Ave. Dr. Arce, 37, 28002 Madrid, Spain. Tel.: +34 91 585 4735; fax: +34 91 585 4754; HHMI, Department of Biological Sciences, 1212 Amsterdam Av., New York, NY 10027, USA. Tel.: +1 212 854 2354; fax: +1 212 854 4619. e-mail: defelipecajal.csic.es; rmy5@ 123456columbia.edu

                aPresent address: Department of Neurobiology, Yale University School of Medicine, New Haven, CT 06520, USA.

                Article
                10.3389/neuro.01.1.1.010.2007
                2518053
                18982124
                fbe239e1-07cf-48fe-9369-14830f9e2293
                Copyright: © 2007 Arellano, Benavides-Piccione, DeFelipe and Yuste.

                This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

                History
                : 15 August 2007
                : 01 September 2007
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 65, Pages: 14, Words: 8336
                Categories
                Neuroscience
                Original Research

                Neurosciences
                serial section,pyramidal,electron microscopy,psd
                Neurosciences
                serial section, pyramidal, electron microscopy, psd

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