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Synapse clusters are preferentially formed by synapses with large recycling pool sizes.

Welzel O, Tischbirek CH, Jung J, Kohler EM, Svetlitchny A, Henkel AW, Kornhuber J, Groemer TW - PLoS ONE (2010)

Bottom Line: Accordingly, vesicle-rich synapses were found to preferentially reside next to neighbours with large recycling pool sizes.Analysis of synapse distributions in these systems confirmed the results obtained with FM 1-43.Our findings support the idea that clustering of synapses with large recycling pool sizes is a distinct developmental feature of newly formed neural networks and may contribute to functional plasticity.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Psychotherapy, University of Erlangen-Nuremberg, Erlangen, Germany.

ABSTRACT
Synapses are distributed heterogeneously in neural networks. The relationship between the spatial arrangement of synapses and an individual synapse's structural and functional features remains to be elucidated. Here, we examined the influence of the number of adjacent synapses on individual synaptic recycling pool sizes. When measuring the discharge of the styryl dye FM1-43 from electrically stimulated synapses in rat hippocampal tissue cultures, a strong positive correlation between the number of neighbouring synapses and recycling vesicle pool sizes was observed. Accordingly, vesicle-rich synapses were found to preferentially reside next to neighbours with large recycling pool sizes. Although these synapses with large recycling pool sizes were rare, they were densely arranged and thus exhibited a high amount of release per volume. To consolidate these findings, functional terminals were marked by live-cell antibody staining with anti-synaptotagmin-1-cypHer or overexpression of synaptopHluorin. Analysis of synapse distributions in these systems confirmed the results obtained with FM 1-43. Our findings support the idea that clustering of synapses with large recycling pool sizes is a distinct developmental feature of newly formed neural networks and may contribute to functional plasticity.

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Relation of recycling pool size and number of neighbours.A, Analytical image calculated from a representative FM 1–43 turnover experiment. Each detected synapse is marked by a filled circle, which is gray-shaded according to its recycling pool size and size-coded for its number of neighbours in a 50 µm2 environment. (For the original difference image of images before and after electrical stimulation see Figure S2). B, Relation of recycling pool sizes and neighbour numbers in 30 independent FM 1–43 turnover experiments. Each experiment is represented by an individually coloured line. There was a strong correlation between pool size and number of neighbours that was conserved in all individual experiments (N = 30; mean Spearman's ρ = 0.97±0.03, p<0.01). C, Summary graph of B. Black circles: Relation between number of neighbours and vesicle pool sizes (Cohens d = 4.76; Spearman's ρ = 0.97, p<0.001). Blue squares: Relation between the number of neighbours and the mean pool size of their neighbouring synapses (Cohens d = 2.30; Spearman's ρ = 0.95, p<0.001). Error bars indicate standard error of the mean (N = 30, n = 22528).
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pone-0013514-g002: Relation of recycling pool size and number of neighbours.A, Analytical image calculated from a representative FM 1–43 turnover experiment. Each detected synapse is marked by a filled circle, which is gray-shaded according to its recycling pool size and size-coded for its number of neighbours in a 50 µm2 environment. (For the original difference image of images before and after electrical stimulation see Figure S2). B, Relation of recycling pool sizes and neighbour numbers in 30 independent FM 1–43 turnover experiments. Each experiment is represented by an individually coloured line. There was a strong correlation between pool size and number of neighbours that was conserved in all individual experiments (N = 30; mean Spearman's ρ = 0.97±0.03, p<0.01). C, Summary graph of B. Black circles: Relation between number of neighbours and vesicle pool sizes (Cohens d = 4.76; Spearman's ρ = 0.97, p<0.001). Blue squares: Relation between the number of neighbours and the mean pool size of their neighbouring synapses (Cohens d = 2.30; Spearman's ρ = 0.95, p<0.001). Error bars indicate standard error of the mean (N = 30, n = 22528).

Mentions: When analyzing the recycling pool size and the number of neighbours of each synapse, we observed that synapses located within synapse clusters contained significantly more recycling vesicles (Figure 2A,C; Wilcoxon rank sum test: p<0.001). Thus, when correlating number of neighbours and recycling pool size, a strong correlation between these parameters was observed in 30 independent experiments (Figure 2B). In principle, this correlation could arise from appraisal artefacts as synapses located in close proximity to each other are more likely to overlap. However, the correlation was still observed for synapses with low number of neighbours. The difference of recycling pool sizes between synapses with, for example, a single neighbour and those with three neighbours is already highly significant (Wilcoxon rank sum test: p<0.001). These synapses reside in sparsely populated areas of the culture and their overlap on the acquired image is unlikely.


Synapse clusters are preferentially formed by synapses with large recycling pool sizes.

Welzel O, Tischbirek CH, Jung J, Kohler EM, Svetlitchny A, Henkel AW, Kornhuber J, Groemer TW - PLoS ONE (2010)

Relation of recycling pool size and number of neighbours.A, Analytical image calculated from a representative FM 1–43 turnover experiment. Each detected synapse is marked by a filled circle, which is gray-shaded according to its recycling pool size and size-coded for its number of neighbours in a 50 µm2 environment. (For the original difference image of images before and after electrical stimulation see Figure S2). B, Relation of recycling pool sizes and neighbour numbers in 30 independent FM 1–43 turnover experiments. Each experiment is represented by an individually coloured line. There was a strong correlation between pool size and number of neighbours that was conserved in all individual experiments (N = 30; mean Spearman's ρ = 0.97±0.03, p<0.01). C, Summary graph of B. Black circles: Relation between number of neighbours and vesicle pool sizes (Cohens d = 4.76; Spearman's ρ = 0.97, p<0.001). Blue squares: Relation between the number of neighbours and the mean pool size of their neighbouring synapses (Cohens d = 2.30; Spearman's ρ = 0.95, p<0.001). Error bars indicate standard error of the mean (N = 30, n = 22528).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2958124&req=5

pone-0013514-g002: Relation of recycling pool size and number of neighbours.A, Analytical image calculated from a representative FM 1–43 turnover experiment. Each detected synapse is marked by a filled circle, which is gray-shaded according to its recycling pool size and size-coded for its number of neighbours in a 50 µm2 environment. (For the original difference image of images before and after electrical stimulation see Figure S2). B, Relation of recycling pool sizes and neighbour numbers in 30 independent FM 1–43 turnover experiments. Each experiment is represented by an individually coloured line. There was a strong correlation between pool size and number of neighbours that was conserved in all individual experiments (N = 30; mean Spearman's ρ = 0.97±0.03, p<0.01). C, Summary graph of B. Black circles: Relation between number of neighbours and vesicle pool sizes (Cohens d = 4.76; Spearman's ρ = 0.97, p<0.001). Blue squares: Relation between the number of neighbours and the mean pool size of their neighbouring synapses (Cohens d = 2.30; Spearman's ρ = 0.95, p<0.001). Error bars indicate standard error of the mean (N = 30, n = 22528).
Mentions: When analyzing the recycling pool size and the number of neighbours of each synapse, we observed that synapses located within synapse clusters contained significantly more recycling vesicles (Figure 2A,C; Wilcoxon rank sum test: p<0.001). Thus, when correlating number of neighbours and recycling pool size, a strong correlation between these parameters was observed in 30 independent experiments (Figure 2B). In principle, this correlation could arise from appraisal artefacts as synapses located in close proximity to each other are more likely to overlap. However, the correlation was still observed for synapses with low number of neighbours. The difference of recycling pool sizes between synapses with, for example, a single neighbour and those with three neighbours is already highly significant (Wilcoxon rank sum test: p<0.001). These synapses reside in sparsely populated areas of the culture and their overlap on the acquired image is unlikely.

Bottom Line: Accordingly, vesicle-rich synapses were found to preferentially reside next to neighbours with large recycling pool sizes.Analysis of synapse distributions in these systems confirmed the results obtained with FM 1-43.Our findings support the idea that clustering of synapses with large recycling pool sizes is a distinct developmental feature of newly formed neural networks and may contribute to functional plasticity.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Psychotherapy, University of Erlangen-Nuremberg, Erlangen, Germany.

ABSTRACT
Synapses are distributed heterogeneously in neural networks. The relationship between the spatial arrangement of synapses and an individual synapse's structural and functional features remains to be elucidated. Here, we examined the influence of the number of adjacent synapses on individual synaptic recycling pool sizes. When measuring the discharge of the styryl dye FM1-43 from electrically stimulated synapses in rat hippocampal tissue cultures, a strong positive correlation between the number of neighbouring synapses and recycling vesicle pool sizes was observed. Accordingly, vesicle-rich synapses were found to preferentially reside next to neighbours with large recycling pool sizes. Although these synapses with large recycling pool sizes were rare, they were densely arranged and thus exhibited a high amount of release per volume. To consolidate these findings, functional terminals were marked by live-cell antibody staining with anti-synaptotagmin-1-cypHer or overexpression of synaptopHluorin. Analysis of synapse distributions in these systems confirmed the results obtained with FM 1-43. Our findings support the idea that clustering of synapses with large recycling pool sizes is a distinct developmental feature of newly formed neural networks and may contribute to functional plasticity.

Show MeSH
Related in: MedlinePlus