A new efficient method for synaptic vesicle quantification reveals differences between medial prefrontal cortex perforated and nonperforated synapses

Journal of Comparative Neurology

Volumn 522, Issue 2, 2014, Pages 284-297

  Nava, Nicoletta ^a,b   Chen, Fenghua ^a,b   Wegener, Gregers ^b,d   Popoli, Maurizio ^c   Nyengaard, Jens Randel ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF MILAN   (Italy)

^d NORTH WEST UNIVERSITY   (South Africa)

Author keywords

Cavalieri estimator; Glutamate; Number estimation; Serial section electron microscopy; Synaptic plasticity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; LIMIT OF QUANTITATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; NONPERFORATED SYNAPSE; PERFORATED SYNAPSE; POSTSYNAPTIC DENSITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STEREOLOGY; SYNAPSE VESICLE; SYNAPTOSOME; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY;

CAVALIERI ESTIMATOR; GLUTAMATE; NUMBER ESTIMATION; SERIAL SECTION ELECTRON MICROSCOPY; SYNAPTIC PLASTICITY;

ANIMALS; IMAGING, THREE-DIMENSIONAL; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; SYNAPTIC VESICLES;

EID: 84889682453     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23482     Document Type: Article

References (50)

1. Arnsten AF, Li BM. 2005. Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biol Psychiatry57:1377-1384.
2. Bekkers JM, Richerson GB, Stevens CF. 1990. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc Natl Acad Sci U S A87:5359-5362.
3. Bourne JN, Harris KM. 2011. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus21:354-373.
4. Colonnier M. 1968. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res9:268-287.
5. Cruz-Orive LM. 1983. Distribution-free estimation of sphere size distributions from slabs showing overprojection and truncation, with a review of previous methods. J Microsc131:265-290.
6. DeFelipe J, Alonso-Nanclares L, Arellano JI. 2002. Microstructure of the neocortex: comparative aspects. J Neurocytol31:299-316.
7. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron18:995-1008.
8. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ. 2001. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc204:232-46.
9. Dosemeci A, Tao-Cheng JH, Vinade L, Winters CA, Pozzo-Miller L, Reese TS. 2004. Glutamate-induced transient modification of the postsynaptic density. Proc Natl Acad Sci U S A98:10428-10432.
10. Douglas RJ, Martin KA. 2007. Mapping the matrix: the ways of neocortex. Neuron56:226-238.
11. Fatt P, Katz B. 1952. Spontaneous subthreshold activity at motor nerve endings. J Physiol117:109-128.
12. Fiala JC, Harris KM. 2001. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J Microsc202:468-472.
13. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. 2004a. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol468:86-95.
14. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. 2004b. Synapses with a segmented, completely partitioned postsynaptic density express more AMPA receptors than other axospinous synaptic junctions. Neuroscience125:615-623.
15. Geinisman Y. 1993. Perforated axospinous synapses with multiple, completely partitioned transmission zones: probable structural intermediates in synaptic plasticity. Hippocampus3:417-433.
16. Gray EG. 1959a. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat93:420-433.
17. Gray EG. 1959b. Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature183:1592-1593.
18. Gundersen HJ. 2002. The smooth fractionator. J Microsc207:191-210.
19. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc147:229-263.
20. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B. 1988. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. AMPIS96:857-881.
21. Gundersen HJ, Jensen EB, Kieu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology-reconsidered. J Microsc193:199-211.
22. Harris KM. 1999. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol9:343-348.
23. Harris KM, Sultan P. 1995. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology34:1387-1395.
24. Harris KM, Jensen FE, Tsao B. 1992. 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 Neurosci12:2685-2705.
25. Harris KM, Perry E, Bourne J, Feinberg M, Ostroff L, Hurlburt J. 2006. Uniform serial sectioning for transmission electron microscopy. J Neurosci26:12101-12103.
26. Hu Y, Qu L, Schikorski T. 2008. Mean synaptic vesicle size varies among individual excitatory hippocampal synapses. Synapse62:953-957.
27. Knott G, Marchman H, Wall D, Lich B. 2008. Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J Neurosci28:2959-2964.
28. Kuwajima M, Mendenhall JM, Harris KM. 2013. Large-volume reconstruction of brain tissue from high-resolution serial section images acquired by SEM-based scanning transmission electron microscopy. Methods Mol Biol950:253-173.
29. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B. 1997. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol500:409-440.
30. Miranda R, Nudel U, Laroche S, Vaillend C. 2011. Altered presynaptic ultrastructure in excitatory hippocampal synapses of mice lacking dystrophins Dp427 or Dp71. Neurobiol Dis43:134-141.
31. Mishchenko Y, Hu T, Spacek J, Mendenhall J, Harris KM, Chklovskii DB. 2010. Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron67:1009-1020.
32. Moghaddam B. 1993. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem60:1650-1657.
33. Mozhayeva MG, Sara Y, Liu X, Kavalali ET. 2002. Development of vesicle pools during maturation of hippocampal synapses. J Neurosci22:654-665.
34. Neves G, Cooke SF, Bliss TV. 2008. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci9:65-75.
35. Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y. 2006. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron50:431-442.
36. Nyengaard JR. 1999. Stereologic methods and their application in kidney research. J Am Soc Nephrol10:1100-1123.
37. Ostroff LE, Cain CK, Jindal N, Dar N, Ledoux JE. 2012. Stability of presynaptic vesicle pools and changes in synapse morphology in the amygdala following fear learning in adult rats. J Comp Neurol520:295-314.
38. Qu L, Akbergenova Y, Hu Y, Schikorski T. 2009. Synapse-to-synapse variation in mean synaptic vesicle size and its relationship with synaptic morphology and function. J Comp Neurol514:343-352.
39. Rasmusson A, Hahn U, Larsen JO, Gundersen HJ, Jensen EB, Nyengaard JR. 2013. The spatial rotator. J Microsc250:88-100.
40. Sametsky EA, Disterhoft JF, Geinisman Y, Nicholson DA. 2010. Synaptic strength and postsynaptically silent synapses through advanced aging in rat hippocampal CA1 pyramidal neurons. Neurobiol Aging31:813-825.
41. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci17:5858-5867.
42. Schikorski T, Stevens CF. 1999. Quantitative fine-structural analysis of olfactory cortical synapses. Proc Natl Acad Sci U S A96:4107-4112.
43. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci4:391-395.
44. Small JV. 1968.Measurement of section thickness. Fourth European Conference on Electron Microscopy, pp 609-610.
45. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc134:127-136.
46. Sudhof TC. 2000. The synaptic vesicle cycle revisited. Neuron28:317-320.
47. Tyler WJ, Pozzo-Miller LD. 2001. BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci21:4249-4258.
48. Uylings HB, van Eden CG. 1990. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res85:31-62.
49. Valdivia O. 1971. Methods of fixation and the morphology of synaptic vesicles. J Comp Neurol142:257-273.
50. Van Eden CG, Uylings HB. 1985. Cytoarchitectonic development of the prefrontal cortex in the rat. J Comp Neurol241:253-267.