Age-based comparison of human dendritic spine structure using complete three-dimensional reconstructions

Cerebral Cortex

Volumn 23, Issue 8, 2013, Pages 1798-1810

  Benavides Piccione, Ruth ^a,b,d   Fernaud Espinosa, Isabel ^b   Robles, Victor ^c   Yuste, Rafael ^e   Defelipe, Javier ^a,b,d  

^a INSTITUTO CAJAL   (Spain)

^b Laboratorio Cajal de Circuitos Corticales (CTB)   (United States)

^c UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^e Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

3D reconstructions; cerebral cortex; confocal; intracellular; Lucifer Yellow

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BRAIN TISSUE; CELL STRUCTURE; CINGULATE GYRUS; DATA BASE; DENDRITIC SPINE; FLUORESCENCE MICROSCOPE; HUMAN; HUMAN TISSUE; IMAGE RECONSTRUCTION; LASER MICROSCOPE; MALE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; THREE DIMENSIONAL IMAGING; TISSUE FIXATION;

3D RECONSTRUCTIONS; CEREBRAL CORTEX; CONFOCAL; INTRACELLULAR; LUCIFER YELLOW;

ADULT; AGE FACTORS; AGED, 80 AND OVER; DENDRITIC SPINES; HUMANS; IMAGING, THREE-DIMENSIONAL; MALE; PYRAMIDAL CELLS;

EID: 84880207021     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs154     Document Type: Article

References (48)

1. Anderson K, Bones B, Robinson B, Hass C, Lee H, Ford K, Roberts TA, Jacobs B. 2009. The morphology of supragranular pyramidal neurons in the human insular cortex: a quantitative Golgi study. Cerebral Cortex. 19:2131-2144.
2. Araya R, Jiang J, Eisenthal KB, Yuste R. 2006. The spine neck filters membrane potentials. Proc Natl Acad Sci USA. 103:17961-17966.
3. Arellano JI, Benavides-Piccione R, DeFelipe J, Rafael Yuste R. 2007. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci. 1:131-143.
4. Arellano JI, Espinosa A, Fairén A, Yuste R, DeFelipe J. 2007. Non-synaptic dendritic spines in neocortex. Neuroscience. 145:464-469.
5. Ballesteros-Yáñez I, Benavides-Piccione R, Bourgeois JP, Changeux JP, DeFelipe J. 2010. Alterations of cortical pyramidal neurons in mice lacking high-affinity nicotinic receptors. Proc Natl Acad Sci USA. 107:11567-11572.
6. Ballesteros-Yáñez I, Benavides-Piccione R, Elston G, Yuste R, DeFelipe J. 2006. Density and morphology of dendritic spines in mouse neocortex. Neuroscience. 138:403-409.
7. Benavides-Piccione R, Ballesteros-Yáñez I, DeFelipe J, Yuste R. 2002. Cortical area and species differences in dendritic spine morphology. J Neurocytol. 31:337-346.
8. Blazquez-Llorca L, Garcia-Marín V, DeFelipe J. 2010. Pericellular innervation of neurons expressing abnormally hyperphosphory-lated tau in the hippocampal formation of Alzheimer's disease patients. J Front Neuroanat. 4:20.
9. Bonhoeffer T, Yuste R. 2002. Spine motility. Phenomenology, mechanisms, and function. Neuron. 35:1019-1027.
10. Braak H, Braak E. 1991. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82:239-259.
11. DeFelipe J. 2011. The evolution of the brain, the human nature of cortical circuits and intellectual creativity. Front Neuroanat. 5:29.
12. Dumitriu D, Hao J, Hara Y, Kaufmann J, Janssen WG, Lou W, Rapp PR, Morrison JH. 2010. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci. 30:7507-7515.
13. Dunaevsky A, Tashiro A, Majewska A, Mason CA, Yuste R. 1999. Developmental regulation of spine motility in mammalian CNS. Proc Natl Acad Sci USA. 96:13438-13443.
14. Elston GN. 2007. Specializations in pyramidal cell structure during primate evolution. In: Kaas JH, Preuss TM, editors. Evolution of nervous systems. Vol. 4. Oxford: Academic. p 191-242.
15. Elston GN, Benavides-Piccione R, DeFelipe J. 2001. The pyramidal cell in cognition: A comparative study in human and monkey. Journal of Neuroscience. 21:RC163.
16. Elston GN, Benavides-Piccione R, Elston A, Manger PR, DeFelipe J. 2011. Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species. Front Neuroanat. 5:2. doi: 10.3389/fnana.2011.00002.
17. Elston GN, DeFelipe J. 2002. Spine distribution in cortical pyramidal cells: a common organizational principle across species. Prog Brain Res. 136:109-133.
18. Elston GN, Rosa MG. 1997. The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex. 7:432-452.
19. Feldman ML, Peters A. 1979. A technique for estimating total spine numbers on Golgi impregnated dendrites. J Comp Neurol. 188:527-542.
20. Garey LJ. 1994. Brodmann's localisation in the cerebral cortex. London (UK): Smith-Gordon.
21. 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 Neurosci. 12:2685-2705.
22. Harris KM, Stevens JK. 1989. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci. 9:2982-2997.
23. Hof PR, Morrison JH. 2004. The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci. 27:607-613 (Review).
24. Jacobs B, Driscoll L, Schall M. 1997. Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol. 386:661-680.
25. Jacobs B, Schall M, Prather M, Kapler L, Driscoll L, Baca S, Jacobs J, Ford K, Wainwright M, Treml M. 2001. Regional dendritic and spine variation in human cerebral cortex: a quantitative study. Cereb Cortex. 11:558-571.
26. Jacobs B, Scheibel AB. 2002. Regional dendritic variation in primate cortical pyramidal cells. In: Schüz A, Miller R, editors. Cortical areas: unity and diversity. London (UK): Taylor & Francis. p. 111-131.
27. Jones EG, Powell TPS. 1969. Morphological variation in the dendritic spines of the neocortex. J Cell Sci. 5:509-529.
28. Kabaso D, Coskren PJ, Henry BI, Hof PR, Wearne SL. 2009. The elec-trotonic structure of pyramidal neurons contributing to prefrontal cortical circuits in macaque monkeys is significantly altered in aging. Cereb Cortex. 19:2248-2268.
29. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J. 2010. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 33:121-129.
30. Konur S, Rabinowitz D, Fenstermaker V, Yuste R. 2003. Systematic regulation of spine head diameters and densities in pyramidal neurons from juvenile mice. J Neurobiol. 56:95-112.
31. Majewska A, Brown E, Ross J, Yuste R. 2000. Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci. 20:1722-1734.
32. Majewska A, Tashiro A, Yuste R. 2000. Regulation of spine calcium compartmentalization by rapid spine motility. J Neurosci. 20:8262-8268.
33. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
34. Matus A. 2000. Actin-based plasticity in dendritic spines. Science 290:754-758.
35. Megias M, Emri Z, Freund TF, Gulyas AI. 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540.
36. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L. 1991. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology. 41:479-486.
37. Miura K, Tsubo Y, Okada M, Fukai T. 2007. Balanced excitatory and inhibitory inputs to cortical neurons decouple firing irregularity from rate modulations. J Neurosci. 27:13802-13812.
38. Nusser Z, Lujan R, Laube G, Roberts J, Molnar E, Somogyi P. 1998. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron. 21:545-559.
39. Petanjek Z, Judas M, Kostović I, Uylings HB. 2008. Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefron-tal cortex: a layer-specific pattern. Cereb Cortex. 18:915-929.
40. Petanjek Z, Judaš M, Šimic G, Rasin MR, Uylings HB, Rakic P, Kosto-vic I. 2011. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA. 108:13281-13286.
41. Rakic P, Bourgeois JP, Goldman-Rakic PS. 1994. Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. Prog Brain Res. 102:227-243 (Review).
42. Rall W. 1959. Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol. 1:491-527.
43. Rall W. 1995. In: Segev I., Rinzel J., Shepherd G. editors. The theoretical foundation of dendritic function. Massachusetts: MIT Press.
44. Schikorski T, Stevens C. 1999. Quantitative fine-structural analysis of olfactory cortical synapses. Proc Natl Acad Sci USA. 96:4107-4112.
45. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci. 4:391-395.
46. Spacek J, Hartmann M. 1983. Three-dimensional analysis of dendritic spines. I. Quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices. Anat Embryol. 167:289-310.
47. Yuste R. 2010. Dendritic spines. Cambridge (MA): MIT Press.
48. Yuste R, Majewska A, Holthoff K. 2000. From form to function: calcium compartmentalization in dendritic spines. Nat Neurosci. 3:653-659.