Microtubules, dendritic spines and spine apparatuses

Westrum, Lesnick E.; Jones, D. Hugh; Gray, Edward G.; Barron, Julie

doi:10.1007/bf00234868

Cited by 97 publications

(67 citation statements)

References 19 publications

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“…4 A, B), which is a membranous organelle that connects the synapse to the smooth endoplasmic reticulum in the dendrite (Westrum et al, 1980;Spacek, 1985; A, Electron micrographs of polyribosomes (arrows) in a dendritic shaft (A1) and in a dendritic spine base (A2), neck (A3), and head (A4 ). Arrowheads indicate synapses on the spines in A3 and A4.…”

Section: Resultsmentioning

confidence: 99%

Accumulation of Polyribosomes in Dendritic Spine Heads, But Not Bases and Necks, during Memory Consolidation Depends on Cap-Dependent Translation Initiation

et al. 2017

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Translation in dendrites is believed to support synaptic changes during memory consolidation. Although translational control mechanisms are fundamental mediators of memory, little is known about their role in local translation. We previously found that polyribosomes accumulate in dendritic spines of the adult rat lateral amygdala (LA) during consolidation of aversive pavlovian conditioning and that this memory requires cap-dependent initiation, a primary point of translational control in eukaryotic cells. Here we used serial electron microscopy reconstructions to quantify polyribosomes in LA dendrites when consolidation was blocked by the cap-dependent initiation inhibitor 4EGI-1. We found that 4EGI-1 depleted polyribosomes in dendritic shafts and selectively prevented their upregulation in spine heads, but not bases and necks, during consolidation. Cap-independent upregulation was specific to spines with small, astrocyteassociated synapses. Our results reveal that cap-dependent initiation is involved in local translation during learning and that local translational control varies with synapse type.

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Section: Resultsmentioning

confidence: 99%

Accumulation of Polyribosomes in Dendritic Spine Heads, But Not Bases and Necks, during Memory Consolidation Depends on Cap-Dependent Translation Initiation

et al. 2017

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“…Perforated PSDs are thought to be a site of synaptic plasticity, as their number increases during axonal regeneration and LTP and they are required for learning in aged rats (Nieto-Sampedro et al, 1982;Desmond and Levy, 1986Geinisman et al, 1986). The sacs of SER in the spine apparatus are thought to sequester calcium Fitkova et al, 1983;Andrews et al, 1988;Mignery et al, 1989), and the densestaining material between the sacs of a mature spine apparatus is thought to be of microtubular origin and possibly to serve both structural and protein synthetic roles (Westrum et al, 1980;Spacek, 1985a,b). These interpretations suggest that the parallel maturation of the spine apparatus with the occurrence of the perforated PSDs could signal an enhanced regulation of ionic fluxes and protein synthesis in the large adult mushroom spines.…”

Section: Discussionmentioning

confidence: 99%

Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation [published erratum appears in J Neurosci 1992 Aug;12(8):following table of contents]

1992

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It has long been hypothesized that changes in dendritic spine structure may modify the physiological properties of synapses located on them. Due to their small size, large number, and highly variable shapes, standard light microscopy of Golgi impregnations and electron microscopy (EM) of single thin sections have not proved adequate to identify most spines in a sample or to quantify their structural dimensions and composition. Here we describe a new approach, the series sample, that was developed to classify by shape and subcellular composition all of the spines and synapses in a sample of neuropil by viewing them through serial EM sections. Spines in each class are then randomly selected for serial reconstruction and measurement in three dimensions. This approach was used to assess whether structural changes in hippocampal CA1 spines could contribute to the enhanced synaptic transmission and the greater endurance of long-term potentiation (LTP) that occur with maturation. Our results show a near doubling in the total density of synapses in the neuropil and along reconstructed dendrites between postnatal day 15 (PND 15) and adult ages. However, this doubling does not occur uniformly across all spine and synapse morphologies. Thin spines, mushroom spines containing perforated postsynaptic densities (PSDs) and spine apparatuses, and branched spines increase by about four-fold in density between PND 15 and adult ages. In contrast, stubby spines decrease by more than half and no change occurs in mushroom spines with macular PSDs or in dendritic shaft synapses. The stubby spines that remain are smaller in adults than at PND 15 and the mushroom spines are larger, while no change occurs in the three-dimensional structure of thin spines. Only a few spine necks at either age are constricted or long enough to attenuate charge transfer; therefore, the doubling in synapses should mediate the enhancement of synaptic transmission that occurs with maturation. In addition, LTP is not likely to be mediated by widening of spine necks at either age. However, the constricted spine necks could serve to concentrate specific molecules at activated synapses, thereby enhancing the specificity and endurance of LTP with maturation. These results demonstrate that the new series sample method combined with three- dimensional reconstruction reveals quantitative changes in the frequency and structure of spines and synapses that are not discernable by other methods and are likely to have dramatic effects on synaptic physiology and plasticity.

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“…The spine apparatus, which we visualize to play a role in the division of synapses, is an aggregation of cisternae within the dendritic spine, with electron opaque material appearing between adjacent cisternae (2,22,43,44). Indeed, Tarrant and Routtenberg (20) have shown the presence of filamentous connections and membranous extensions between the spine apparatus, the synaptic spinule, and the PSD, leading them to propose that all of these structures are intimately related to one another.…”

mentioning

confidence: 92%

Plasticity in the central nervous system: do synapses divide?

Carlin¹,

Siekevitz²

1983

Proc. Natl. Acad. Sci. U.S.A.

192

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Changes in the proportion of synapses containing postsynaptic densities with perforations during periods of increased synapse formation have led us to propose a hypothesis describing a possible division of preexisting synapses. Relevant features of this model are that various types of stimulation result in the following sequence of events: (i) the synaptic junction increases in area; (ii) a perforation forms in the enlarging synaptic junction; (iW) a synaptic spinule appears apposed to the perforation in the postsynaptic density; (iv) the perforation in the synaptic junction increases in size until the synaptic junction splits into two separate synapticjunctions within the same synaptic terminal; and (v) the dendritic spine divides into two, each containing a synaptic junction. Physiological responses in which synapse division may possibly play a role include hormone-induced neuronal changes, reinnervation of dendrites after lesions, and learning and memory.Knowledge about plasticity, defined as any persistent change in the functional properties of single neurons or neuronal networks, is a prerequisite for the neurophysiological study of learning. Many mechanisms have been proposed to account for plasticity, including changes in synaptic potential, axonal sprouting and the formation of new synapses, synaptic degeneration, and reverberatory circuits (1). It is highly unlikely that there is a single major mechanism responsible for plasticity, but instead plasticity can result from a number of mechanisms. We would like to propose another possible mechanism in which the division of preexisting synapses can increase the number of synaptic contacts between two neurons. The basis for such a proposal is the structure of the postsynaptic density (PSD).The PSD is a disk-shaped subcellular organelle (diameter, 100-900 nm), which appears as a thickening of electron-dense material attached to the postsynaptic membrane of synaptic junctions (2). One of the features of these PSDs is that they occasionally contain one, or sometimes more, large hole or perforation in their structure giving them a torus or doughnut-shaped morphology (3-5). We will refer to those PSDs containing holes as perforated PSDs and those without as nonperforated PSDs. Although the function of the perforation is unknown, we believe that this configuration may represent an intermediate in the process of synapse division. Whenever there occurs a large perforation in the PSD, no cleft material, presynaptic dense projections, or synaptic vesicles have been viewed apposed to this perforation (5-7). Because the PSD is tightly coupled to the presynaptic side of the synapse (3,8), any change in the morphology of the PSD or presynaptic grid is reflected in a change in the morphology of the entire synapse.We would now like to present evidence, discussed in detail later, which supports the concept of synapse division (see Fig. 1): (i) increases in synapse number have been found to be correlated with an increase in the proportion of synapses containing PSD...

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Microtubules, dendritic spines and spine apparatuses

Cited by 97 publications

References 19 publications

Accumulation of Polyribosomes in Dendritic Spine Heads, But Not Bases and Necks, during Memory Consolidation Depends on Cap-Dependent Translation Initiation

Accumulation of Polyribosomes in Dendritic Spine Heads, But Not Bases and Necks, during Memory Consolidation Depends on Cap-Dependent Translation Initiation

Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation [published erratum appears in J Neurosci 1992 Aug;12(8):following table of contents]

Plasticity in the central nervous system: do synapses divide?

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