Three-dimensional reconstruction of synapses and dendritic spines in the rat and ground squirrel hippocampus: New structural-functional paradigms for synaptic function

Abstract

Vinogradova has published a review [1] addressing the state of neuroscience at the change of one of millennium to the next and the paradigm shift in relation to the interactions both between neurons and between neurons and glial cells. We believe there is a need to supplement this information with further data on synapses, which underlie the operation of the mammalian brain, and this is the aim of the present article, which reviews recently published data and our own work.Traditionally, the questions of learning, memory, and forgetting are linked to neuronal plasticity, which is based on changes in synapses. The term "synapse" (from the Greek synapsis, meaning junction) was introduced by Foster and Sherrington at the end of the 19th century [22] and means "connection." The term subsequently acquired wide use in the contemporary sense to identify connections between neurons [47]. According to [5,6], plasticity can arbitrarily be divided into two categories: 1) changes in already-existing synapses without changes in neuronal connections [71] and 2) changes in interneuronal connections due to the de novo formation and disappearance of synapses [52]. The "chemical synapse" is an area of contact between a dendrite and the presynaptic part or "presynaptic bouton" of an axon and contains vesicles containing neurotransmitter, whose release into the synaptic cleft activates the postsynaptic membrane, for example a spine membrane. Neuroscience and Behavioral Physiology, Vol. 35, No. 4, 2005 333Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti, Vol. 54, No. 1, pp, 120-129, January-February, 2004. Original article submitted October 17, 2002, accepted October 28, 2002 Published data are reviewed along with our own data on synaptic plasticity and rearrangements of synaptic organelles in the central nervous system. Contemporary laser scanning and confocal microscopy techniques are discussed, along with the use of serial ultrathin sections for in vivo and in vitro studies of dendritic spines, including those addressing relationships between morphological changes and the efficiency of synaptic transmission, especially in conditions of the long-term potentiation model. Different categories of dendritic spines and postsynaptic densities are analyzed, as are the roles of filopodia in originating spines. The role of serial ultrathin sections for unbiased quantitative stereological analysis and threedimensional reconstruction is assessed. The authors' data on the formation of more than two synapses on single mushroom spines on neurons in hippocampal field CA1 are discussed. Analysis of these data provides evidence for new paradigms in both the organization and functioning of synapses.

Chemically induced long‐term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices

“…The appearance of these spines in mice CA1 is similar to that described by Nikonenko et al . (2003) for rat hippocampal organotypic cultures in vitro, and in vivo by Popov et al . (2003, 2004b) within CA1 stratum radiatum of hibernating ground squirrels and dentate gyrus of normothermic rats.…”

“…Although there is no absolute classification of thin and mushroom, a spine was classified as mushroom if its head was appreciably wider than the width of the neck (as in Figs 3, 4 and 5A); thin, if its length was greater than the width of its neck and head (Fig. 5A), and stubby, if the width of the neck was similar to its length (Peters & Kaiserman‐Abramof, 1969; Popov et al ., 2004a,b). Generally here, the volume of a thin spine was approximately ten times less than the volume of a mushroom one.…”

“…We considered a fourth category of segmented PSDs originating from synapses with two or more independent presynaptic boutons, thus forming multiple‐synapse spines. These multiple‐synapse spines have been previously described in vivo in rat and ground squirrel (Popov et al ., 2003; Popov et al ., 2004b) and in vitro in rat organotypic hippocampal slices (Nikonenko et al ., 2003). For determination of volume and surface area of the 3‐D reconstructed spines and PSDs we utilized the software ‘Trace’ which was developed by Drs J. C. Fiala and K. M. Harris (http://synapses.bu.edu), to generate both volume and surface area.…”

Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: A three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities

“…5E, F) which on randomly examined 2D sections can be described as "partitioned" (Geinisman, 2000); and macular PSDs ( Fig. 5G, H; Sorra and Harris, 1998;Harris, 1999;Hering and Sheng, 2001;Popov et al, 2003). PSD sizes, in terms of area and volume, were also measured in the four animal groups, as were the proportions of perforated PSDs (Table 3).…”

Reconstruct: a free editor for serial section microscopy

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