Perforated axospinous synapses with multiple, completely partitioned transmission zones: Probable structural intermediates in synaptic plasticity

Geinisman, Yuri

doi:10.1002/hipo.450030404

Cited by 127 publications

(94 citation statements)

References 35 publications

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“…Along with simple (macular) PSDs, we also detected a significant fraction of synapses with complex (perforated or segmented) shapes, which were, on average, 1.8 times larger than simple ones. Complex PSDs were initially described at excitatory synapses on dendritic spines, where they are present under control conditions (Harris et al, 1992), but increase in number following induction of plasticity (Geinisman, 1993;Toni et al, 1999Toni et al, , 2001Ganeshina et al, 2004;Stewart et al, 2005). They have been therefore considered as a plausible morphological correlate of synapse strengthening, possibly reflecting the increased number of AMPA receptors expressed at potentiated synapses (Bourne and Harris, 2008).…”

Section: Discussionmentioning

confidence: 99%

Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells

et al. 2011

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This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues.Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. Synaptic activity, such as long-term potentiation (LTP), has been shown to induce morphological plasticity of excitatory synapses on dendritic spines through the spine head and postsynaptic density (PSD) enlargement and reorganization. Much less, however, is known about activity-induced morphological modifications of inhibitory synapses. Using an in vitro model of rat organotypic hippocampal slice cultures and electron microscopy, we studied activity-related morphological changes of somatic inhibitory inputs triggered by a brief oxygeneglucose deprivation (OGD) episode, a condition associated with a synaptic enhancement referred to as anoxic LTP and a structural remodeling of excitatory synapses. Threedimensional reconstruction of inhibitory axo-somatic synapses at different times before and after brief OGD revealed important morphological changes. The PSD area significantly and markedly increased at synapses with large and complex PSDs, but not at synapses with simple, macular PSDs. Activity-related changes of PSD size and presynaptic bouton volume developed in a strongly correlated manner. Analyses of single and serial sections further showed that the density of inhibitory synaptic contacts on the cell soma did not change within 1 h after OGD. In contrast, the proportion of the cell surface covered with inhibitory PSDs, as well as the complexity of these PSDs significantly increased, with less macular PSDs and more complex, segmented shapes. Together, these data reveal a rapid activity-related restructuring of somatic inhibitory synapses characterized by an enlargement and increased complexity of inhibitory PSDs, providing a new mechanism for a quick adjustment of the excitatoryeinhibitory balance. This article is part of a Special Issue entitled 'Synaptic Plasticity & Interneurons'.

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Section: Discussionmentioning

confidence: 99%

Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells

et al. 2011

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“…This may explain why striatal neurons that fire in association with movement commonly do not fire before movement onset (Jaeger et al, 1995;Mink, 1996). The larger size of PT-type terminals than IT-type and their tendency to be apposed to perforated postsynaptic densities may augment their synaptic efficacy (Geinisman, 1993;Sulzer and Pothos, 2000). This might explain why striato-GP neurons appear more responsive to cortical input than striato-EP-SNr neurons (Uhl et al, 1988;Parthasarathy and Graybiel 1997) and more avidly take up and anterogradely transmit the cortically injected H129 strain of herpes simplex virus (Zemanick et al, 1991).…”

Section: Functional Implicationsmentioning

confidence: 99%

“…This might explain why striato-GP neurons appear more responsive to cortical input than striato-EP-SNr neurons (Uhl et al, 1988;Parthasarathy and Graybiel 1997) and more avidly take up and anterogradely transmit the cortically injected H129 strain of herpes simplex virus (Zemanick et al, 1991). Perforated postsynaptic densities also indicate sites of synaptic potentiation (Geinisman, 1993;Geinisman et al, 1996;Sulzer and Pothos, 2000;Topni et al, 2001). Because the basal ganglia is involved in motor learning (Calabresi et al, 1992;Marsden and Obeso, 1994;Gabrieli, 1995;Graybiel and Kimura, 1995), the PT input to striato-GP neurons may participate in learned suppression of conflicting movements.…”

Section: Functional Implicationsmentioning

confidence: 99%

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

Lei

Jiao²,

Mar³

et al. 2004

J. Neurosci.

253

258

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The two main types of corticostriatal neurons are those that project only intratelencephalically (IT-type), the intrastriatal terminals of which are 0.41 m in mean diameter, and those that send their main axon into pyramidal tract and have a collateral projection to striatum (PT-type), the intrastriatal terminals of which are 0.82 m in mean diameter. We used three approaches to examine whether the two striatal projection neuron types (striatonigral direct pathway vs striatopallidal indirect pathway) differ in their input from IT-type and PT-type neurons. First, we retrogradely labeled one striatal projection neuron type or the other with biotinylated dextran amine (BDA)-3000 molecular weight. We found that terminals making asymmetric axospinous contact with striatonigral neurons were 0.43 m in mean diameter, whereas those making asymmetric axospinous contact with striatopallidal neurons were 0.69 m. Second, we preferentially immunolabeled striatonigral neurons for D 1 dopamine receptors or striatopallidal neurons for D 2 dopamine receptors and found that axospinous terminals had a smaller mean size (0.45 m) on D 1 ϩ spines than on D 2 ϩ spines (0.61 m). Finally, we combined selective BDA labeling of IT-type or PT-type terminals with immunolabeling for D 1 or D 2 , and found that IT-type terminals were twice as common as PT-type on D 1 ϩ spines, whereas PT-type terminals were four times as common as IT-type on D 2 ϩ spines. These various results suggest that striatonigral neurons preferentially receive input from IT-type cortical neurons, whereas striatopallidal neurons receive greater input from PT-type cortical neurons. This differential cortical connectivity may further the roles of the direct and indirect pathways in promoting desired movements and suppressing unwanted movements, respectively.

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“…Data have been obtained [61,62] showing that these "spinules" can be present both in the area of the postsynaptic densities (PSD) and around the periphery of the heads of spines. The possible functions of "spinules" are usually assessed in terms of their contribution to the efficiency of synaptic transmission due to increases in the areas of contacts between the pre-and postsynaptic membranes, especially when new spines form [23,25], though experimental data supporting this role for "spinules" in synaptic transmission have yet to be obtained [61]. We note that in the state of cold-induced torpor in the ground squirrel, when brain electrical activity is minimal, "spinules" penetrating into the presynaptic bouton can also be found on the surfaces of dendritic stems [2,3].…”

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confidence: 99%

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

Popov

Deev

Klimenko

et al. 2005

Neurosci Behav Physiol

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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.

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Perforated axospinous synapses with multiple, completely partitioned transmission zones: Probable structural intermediates in synaptic plasticity

Cited by 127 publications

References 35 publications

Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells

Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

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

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