Sampling issues in quantitative analysis of dendritic spines morphology

BMC Bioinformatics

Błażej Ruszczycki¹  Zsuzsanna Szepesi¹  Grzegorz M Wilczynski¹  Monika Bijata¹  Katarzyna Kalita¹  Leszek Kaczmarek¹  Jakub Wlodarczyk¹ 

[1] Nencki Institute of Experimental Biology, Polish Academy of Sciences, Pasteura 3, Warszawa, Poland

关键词: Confocal microsopy;    Synaptic plasticity;    Monte Carlo simulations;    Dendritic spines;   

Others  :  1088157
DOI  :  10.1186/1471-2105-13-213

 received in 2012-05-15, accepted in 2012-08-16,  发布年份 2012

【 摘 要 】

Background

Quantitative analysis of changes in dendritic spine morphology has become an interesting issue in contemporary neuroscience. However, the diversity in dendritic spine population might seriously influence the result of measurements in which their morphology is studied. The detection of differences in spine morphology between control and test group is often compromised by the number of dendritic spines taken for analysis. In order to estimate the impact of dendritic spine diversity we performed Monte Carlo simulations examining various experimental setups and statistical approaches. The confocal images of dendritic spines from hippocampal dissociated cultures have been used to create a set of variables exploited as the simulation resources.

Results

The tabulated results of simulations given in this article, provide the number of dendritic spines required for the detection of hidden morphological differences between control and test groups in terms of spine head-width, length and area. It turns out that this is the head-width among these three variables, where the changes are most easily detected. Simulation of changes occurring in a subpopulation of spines reveal the strong dependence of detectability on the statistical approach applied. The analysis based on comparison of percentage of spines in subclasses is less sensitive than the direct comparison of relevant variables describing spines morphology.

Conclusions

We evaluated the sampling aspect and effect of systematic morphological variation on detecting the differences in spine morphology. The results provided here may serve as a guideline in selecting the number of samples to be studied in a planned experiment. Our simulations might be a step towards the development of a standardized method of quantitative comparison of dendritic spines morphology, in which different sources of errors are considered.

【 授权许可】

   
2012 Ruszczycki et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Yuste R, Denk W: Dendritic spines as basic functional units of neuronal integration. Nature 1995, 375:682-684.
• [2]Segal M: Release of calcium form stores alters the morphology of dendritic spines in cultured hippocampal neurons. Prog Brain Res 2002, 138:53-59.
• [3]Xu T, Xinzhu Yu, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, Zuo Y: Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 2009, 462:915-919.
• [4]Cajal SR: Estructura de los centros nerviosos de las aves. Rev Trimestral de Histologia Normal y Patologica 1888, 1:1-10.
• [5]Segal M: Dendritic spines, synaptic plasticity and neuronal survival”activity shapes dendritic spines to enhance neuronal viability. Eur J Neurosci 2010, 31:2178-2184.
• [6]Yuste R, Bonhoeffer T: Morphological Changes in Dendritic Spines Associated with Long-Term Synaptic Plasticity. Annu Rev Neurosci 2001, 24:1071-1089.
• [7]Zhanga Y, Chena K, Baronc M, Teylanc MA, Kimc Y, Songb Z, Greengardc P, Wong ST: A neurocomputational method for fully automated 3D dendrirtic spine detection and segmentation of medium-sized spiny neurons. Neuroimage 2010, 50:1472-1484.
• [8]Korkotian E, Segal M: Release of calcium form stores alters the morphology of dendritic spines in cultured hippocampal neurons. PNAS 1999, 96:12068-12072.
• [9]Nägerl UV, Willig KI, Hein B, Hell SW, Bonhoeffer T: Live-cell imaging of dendritic spines by STED microscopy. Neural Comput 2008, 105:18982-18987.
• [10]Sala C, Piëch V, Wilson NR, Passafaro M, Liu G, Sheng M: Regulation of Dendritic Spine Morphology and Synaptic Function by Shank and Homer. Neuron 2001, 31:115-130.
• [11]Ballesteros-Yánez I, Benavides-Piccionea R, Elstonb G, Yuste R, DeFelipe J: Density and Morphology of Dendritic Spines in Mouse Neocortex. Neuroscience 2006, 138:403-409.
• [12]Benavides-Piccione R, Ballesteros-Yánez I, DeFelipe J, Yuste R: Cortical area and species differences in dendritic spine morphology. J Neurocytology 2002, 31:337-346.
• [13]Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H: Principles of Long-Term Dynamics of Dendritic Spines. J Neurosci 2008, 28:13592-13608.
• [14]Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H: Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
• [15]Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K: Transient and Persistent Denedritic Spines in the Neurocortex in Vivo. Neuron 2005, 45:279-291.
• [16]Fay MP, Proschan MA: Wilcoxon-Mann-Whitney or t-test? On assumptions for hypothesis tests and multiple interpretations of decision rules. Statist Surv 2010, 4:1-39.
• [17]Ziv N, Smith S: Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 1996, 17:91-102.
• [18]Hering H, Sheng M: Dendritic Spines: Structure, Dynamics and Regulation. Nat Rev Neurosci 2001, 12:880-886.
• [19]Fiala JC, Feinberg M, Popov V, Harris KM: Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal Area CA1. J Neurosci 1998, 18:8900-8911.
• [20]Sorra K, Harris K: Overview on the Structure, Composition, Function, Development, and Plasticity of Hippocampal Dendritic Spines. Hippocampus 2000, 10:501-511.
• [21]Grutzendler J, Kasthuri N, Gan WB: Long-term dendritic spine stability in the adult cortex. Nature 2002, 420:812-816.
• [22]Dailey ME, Smith SJ: The Dynamics of Dendritic Structure in Developing Hippocampal Slices. J Neurosci 1996, 16:2983-2994.
• [23]Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H: Structure-stability-function relationship of dendritic spines. Trends Neurosci 2003, 26:360-368.
• [24]Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguch J: Structral dynamics of dendritic spines in memory and cognition. Trends Neurosci 2003, 33:121-129.
• [25]Hung AY, Futai K, Sala C, Valtschanoff JG, Ryu J, Woodworth MA, Kidd FL, Sung CC, Miyakawa T, Bearand MF, Weinberg RJ, Sheng M: Smaller Dendritic Spines, Weaker Synaptic Transmission, but Enhanced Spatial Learning in Mice Lacking Shank. J Neurosci 2008, 38:1697-1708.
• [26]Jones EG, Powell T: Morphological variations in the den-dritic spines of the neocortex. J Cell Sci 1969, 5:509-529.
• [27]Harris K, Jensen F, Tsao B: 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. J Neurosci 1992, 12:2685-2705.
• [28]Oray S, Majewska A, Sur M: Effects of Synaptic Activity on Dendritic Spine Motility of Developing Cortical Layer V Pyramidal Neurons. Cerebral Cortex 2006, 16:730-741.
• [29]Bergmann R, Ludbrook J, Spooren WPJM: Different Outcomes of the Wilcoxon-Mann-Whitney Test from Different Statistics Packages. Am Statistician 2000, 54:72-77.
• [30]Mann HB, Whitney DR: On a Test of Whether One of Two Random Variables is Stochastically Larger than the Other. Ann Math Statist 1947, 18:50-60.
• [31]Hosokawa T, Rusakov D, Bliss T, Fine A: Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J Neurosci 1995, 15(8):5560-6673.
• [32]Korkotian E, Segal M: Regulation of Dendritic Spine Motility in Cultured Hippocampal Neurons. J Neurosci 2001, 21:6115-6124.
• [33]Ceyhan E: Modeling Metric Distances of Dendrite Spines of Mice Based on Morphometric Measures. In the Proceeding of International Symposium on Health Informatics and Bioinformatics: April 30-May 2, 2007. Edited by Akman LE, Baykal N, Can T, Iscan MUE. Mumcuoglu; 2007. ISBN : 978-975-429-257-2