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

Neuroscience and Behavioral Physiology

Volumn 35, Issue 4, 2005, Pages 333-341

  Popov, V I ^a   Deev, A A ^b   Klimenko, O A ^a   Kraev, I V ^a   Kuz'minykh, S B ^a   Medvedev, N I ^c   Patrushev, I V ^a   Popov, R V ^a   Rogachevskii, V V ^a   Khutsiyan, S S ^a   Stewart, M G ^d   Fesenko, E E ^a  

^a INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^c SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^d OPEN UNIVERSITY   (United Kingdom)

Author keywords

Dendritic spine; Gap junction; Glial cell; Hippocampus; Neuron; Postsynaptic density; Serial ultra thin sections; Synapse; Three dimensional reconstruction

Indexed keywords

CELL ULTRASTRUCTURE; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; DENDRITIC SPINE; FILOPODIUM; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; LASER MICROSCOPY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; REVIEW; SQUIRREL; STEREOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION; THREE DIMENSIONAL IMAGING; TISSUE SECTION; ANIMAL; ARTICLE; COMPARATIVE STUDY; METHODOLOGY; SCIURIDAE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; DENDRITIC SPINES; HIPPOCAMPUS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, ELECTRON, TRANSMISSION; RATS; SCIURIDAE; SYNAPSES;

EID: 21744450287     PISSN: 00970549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11055-005-0030-4     Document Type: Review

References (77)

1. O. S. Vinogradova, "Neuroscience at the end of the second millennium: A paradigm shift," Zh. Vyssh. Nerv. Deyat., 50, No.5, 743-774 (2000).
2. V. I. Popov, N. I. Medvedev, I. V. Patrushev, V. V. Rogachevskii, I. V. Kraev, O. A. Klimenko, D. A. Ignat'ev, S. S. Khutsyan, and M. G. Stewart, "Quantity stereological analysis and 3D reconstruction: Of axodendritic synapses in the hippocampus of the rat and ground squirrel with respect to the efficiency of synaptic transmission," in: Kolosov Readings: IVth International Conference of the Russian Academy of Sciences on Functional Neuromorphology [in Russian], St. Petersburg (2002), pp. 230-231.
3. V. I. Popov, N. I. Medvedev, V. V. Rogachevskii, D. I. Ignat'ev, M. G. Stewart, and E. E. Fesenko, "The three-dimensional organization of synapses and astroglia in the hippocampus of the rat and ground squirrel: New structural-functional paradigms for synapse function," Biofizika, 48, No.2, 289-308 (2003).
4. J. C. Anderson and K. A. Martin, "Does bouton morphology optimize axon length?" Nature Neurosci., 4, No.12, 1166-1167 (2001).
5. C. H. Bailey, M. Giustetto, Y. Y. Huang, R. D. Hawkins, and E. R. Kandel, "Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory?" Nature Rev. Neurosci., 1, No.1, 11-20 (2000).
6. C. H. Bailey and E. R. Kandel, "Structural changes accompanying memory storage," Ann. Rev. Physiol., 55, 397-426 (1993).
7. S. J. Baloyannis, V. Costa, and G. Deretzi, "Intraventricular administration of substance P induces unattached Purkinje cell dendritic spines in rats," Int. J. Neurosci., 62, No.3-4, 251-262 (1992).
8. C. Beaulieu and M. Colonnier, "A laminar analysis of the number of round-asymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat," J. Comp. Neurol., 231, No.2, 180-189 (1985).
9. A. L. Beckman, C. Llados-Beckman, T. L. Stanton, and M. W. Adler, "Differential effect of environmental temperature on morphine physical dependence and abstinence," Life Sci., 30, No.12, 1013-1020 (1982).
10. T. V. Bliss and T. Lomo, "Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path," J. Physiol., 232, No.2, 331-356 (1973).
11. C. Boyer, T. Schikorski, and C. F. Stevens, "Comparison of hippocampal dendritic spines in culture and in brain," J. Neurosci., 18, No.14, 5294-5300 (1998).
12. V. Chan-Palay, "A new synaptic specialization: Filamentous braids," Brain Res., 79, No.2, 280-284 (1974).
13. M. E. Chicurel and K. M. Harris, "Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus," J. Comp. Neurol., 325, No.2, 69-82 (1992).
14. R. E. Coggeshall and H. A. Lekan, "Methods for determining numbers of cells and synapses: A case for more uniform standards of review," J. Comp. Neurol., 364, No.1, 6-15 (1996).
15. M. E. Dailey and S. J. Smith, "The dynamics of dendritic structure in developing hippocampal slices," J. Neurosci., 16, No.9, 2983-2994 (1996).
16. F. Engert and T. Bonhoeffer, "Dendritic spine changes associated with hippocampal long-term synaptic plasticity," Nature, 399, No.6731, 66-70 (1999).
17. J. C. Fiala, B. Allwardt, and K. M. Harris, "Dendritic spines do not split during hippocampal LTP or maturation," Nature Neurosci. 5, No.4, 297-298 (2002).
18. J. C. Fiala, M. Feinberg, V. Popov, and K. M. Harris, "Synaptogenesis via dendritic filopodia in developing hippocampal area CA1," J. Neurosci., 18, No.21, 8900-8911 (1998).
19. J. C. Fiala and K. M. Harris, "Extending unbiased stereology of brain ultrastructure to three-dimensional volumes," J. Am. Med. Inform. Assoc., 8, No.1, 1-16 (2001).
20. E. Fifkova, "Actin in the nervous system," Brain Res., 356, No.2, 187-215 (1985).
21. M. Fischer, S. Kaech, D. Knutti, and A. Matus, "Rapid actin-based plasticity in dendritic spines," Neuron, 20, No.5, 847-854 (1998).
22. M. Foster 1897 Textbook of Physiology The MacMillan Co. New York p. 929
23. Y. Geinisman, "Perforated axospinous synapses with multiple, completely partitioned transmission zones: Probable structural intermediates in synaptic plasticity," Hippocampus, 3, No.4, 417-433 (1993).
24. Y. Geinisman, R. W. Berry, J. F. Disterhoft, J. M. Power, and E. A. Van der Zee, "Associative learning elicits the formation of multiple-synapse boutons," J. Neurosci., 21, No.15, 5568-5573 (2001).
25. Y. Geinisman, L. de Toledo-Morrell, and F. Morrell, "Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segment postsynaptic densities," Brain Res., 566, No.1-2, 77-88 (1991).
26. R. Y. Gordon, L. S. Bocharova, I. I. Kruman, V. I. Popov, A. P. Kazantsev, S. S. Khutzian, and V. N. Karnaukhov, "Acridine orange as an indicator of the cytoplasmic ribosome state," Cytometry, 29, No.3, 215-221 (1997).
27. K. M. Harris, "Calcium from internal stores modifies dendritic spine shape," Proc. Natl. Acad. Sci. USA, 96, No.22, 12213-12215 (1999).
28. K. M. Harris, "Structure, development, and plasticity of dendritic spines," Curr. Opin. Neurobiol., 9, No.3, 343-448 (1999).
29. K. M. Harris, F. E. Jensen, and B. Tsao, "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, No.7, 2685-2705 (1992).
30. K. M. Harris and S. B. Kater, "Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function," Ann. Rev. Neurosci., 17, 341-371 (1994).
31. K. M. Harris and J. K. Stevens, "Dendritic spines of rat cerebellar Purkinje cells: Serial electron microscopy with reference to their bio-physical characteristics," J. Neurosci., 8, No.12, 4455-4469 (1988).
32. H. C. Heller, "Hibernation: Neural aspects," Ann. Rev. Physiol., 41, 305-321 (1979).
33. H. Hering and M. Sheng, "Dendritic spines: Structure, dynamics and regulation," Nature Rev. Neurosci., 2, No.12, 880-888 (2001).
34. C. H. Horner, "Plasticity of the dendritic spine," Prog. Neurobiol., 41, No.3, 281-321 (1993).
35. E. G. Jones and T. P. Powell, "Morphological variations in the dendritic spines of the neocortex," J. Cell Sci., 5, No.2, 509-529 (1969).
36. S. Kaech, H. Parmar, M. Roelandse, C. Bornmann, and A. Matus, "Cytoskeletal microdifferentiation: A mechanism for organizing morphological plasticity in dendrites," Proc. Natl. Acad. Sci. USA, 98, No.13, 7086-7092 (2001).
37. M. B. Kennedy, "The postsynaptic density at glutamatergic synapses," Trends Neurosci., 20, No.6, 264-268 (1997).
38. S. A. Korov and K. M. Harris, "Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated," Nat. Neurosci., 2, No.10, 878-883 (1999).
39. T. Krucker, G. R. Siggins, and S. Halpain, "Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus," Proc. Natl. Acad. Sci. USA, 97, No.12, 6856-6861 (2000).
40. C. P. Lyman J. S. Willis A. Malan and L. C. H. Wang 1982 Hibernation and Torpor in Mammals and Birds Academic Press New York
41. M. Maletic-Savatic, R. Malinow, and K. Svoboda, "Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity," Science, 283, No.5409, 1923-1927 (1999). 10.1126/ science.283.5409.1923
42. G. S. Marrs, S. H. Green, and M. E. Dailey, "Rapid formation and remodeling of postsynaptic densities in developing dendrites," Nat. Neurosci., 4, No.10, 1006-1013 (2001).
43. L. Mihailovic, B. Petrovic-Minic, S. Protic, and I. Divac, "Effects of hibernation on learning and retention," Nature, 218, No.137, 191-192 (1968).
44. J. A. H. H. Murray H. Bradley W. A. Craigie and C. T. Onion 1919 A New English Dictionary on Historical Principles Clarendon Press Oxford
45. L. Ostroff, J. Fiala, B. Allwardt, and K. Harris, "Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices," Neuron, 35, No. 3, 535 (2002).
46. A. Peters and E. G. Jones (eds.), Cerebellar Cortex, Vol. 1: Cellular Components of the Cerebral Cortex, Plenum Press, New York (1984).
47. A. Peters and I. R. Kaiserman-Abramof, "The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines," Am. J. Anat., 127, No.4, 321-355 (1970).
48. A. Peters and S. L. Palay, "The morphology of synapses," J. Neurocytol., 25, No.12, 687-700 (1996).
49. V. I. Popov and L. S. Bocharova, "Hibernation-induced structural changes in synaptic contacts between mossy fibers and hippocampal pyramidal neurons," Neurosci., 48, No.1, 53-60 (1992).
50. V. I. Popov, L. S. Bocharova, and A. G. Bragin, "Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation," Neurosci., 48, No.1, 45-51 (1992).
51. V. I. Popov, D. A. Ignat'ev, and B. Lindemann, "Ultrastructure of taste receptor cells in active and hibernating ground squirrels," J. Electron Microscop. (Tokyo), 48, No.6, 957-969 (1999).
52. S. Ramon-y-Cajal 1995 Histology of Nervous System of Man and Vertebrates Oxford University Press Oxford (English translation by N. Swanson and L. W. Swanson)
53. D. A. Rusakov and D. M. Kullman, "Geometric and viscous components of the tortuosity of the extracellular space in the brain," Proc. Natl. Acad. Sci. USA, 95, No.15, 8975-8980 (1998).
54. C. Sandi, H. A. Davies, M. I. Cordero, J. J. Rodriguez, V. I. Popov, and M. G. Stewart, "Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training," Eur. J. Neurosci., 17 1-10 (2003).
55. M. Segal, "Rapid plasticity of dendritic spine: Hints to possible functions?" Prog. Neurobiol., 63, No.1, 61-70 (2001).
56. M. Segal and P. Aldersen, "Dendritic spines shaped by synaptic activity," Curr. Opin. Neurobiol., 10, No.5, 582-586 (2000).
57. M. Sheng, "Molecular organization of the postsynaptic specialization," Proc. Natl. Acad. Sci. USA, 98, No.13, 7058-7061 (2001).
58. G. M. Shepherd and K. M. Harris, "Three-dimensional structure and composition of CA3-CA1 axons in rat hippocampal slices: Implications for presynaptic connectivity and compartmentalization," J. Neurosci., 18, No.20, 8300-8310 (1998).
59. M. B. Shtark, The Brain of Hibernators, Nauka Novosibirsk (1970); NASA Technical Translations TTF-619 (1972).
60. S. J. Smith, "Neuronal cytomechanics: The actin-based motility of growth cones," Science, 242, No.4879, 708-715 (1988).
61. K. E. Sorra, J. C. Fiala, and K. M. Harris, "Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation," J. Comp. Neurol., 398, No.2, 225-240 (1998).
62. K. E. Sorra and K. M. Harris, "Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines," Hippocampus, 10, No.5, 501-511 (2000).
63. K. E. Sorra and K. M. Harris, "Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1," J. Neurosci., 18, No.2, 658-671 (1998).
64. C. Sotelo, "Cerebellar synaptogenesis: What we can learn from mutant mice," J. Exptl. Biol., 153, 225-249 (1990).
65. J. Spacek and K. M. Harris, "Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat," J. Neurosci., 17, No.1, 190-203 (1997).
66. J. Spacek and K. M. Harris, "Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus," J. Comp. Neurol., 393, No.1, 58-68 (1998).
67. J. Spacek and M. Hartmann, "Three-dimensional analysis of dendritic spines. I. Quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices," Anat. Embryol. (Berlin), 167, No.2, 289-310 (1983).
68. E. N. Star, D. J. Kwiatkowski, and V. N. Murthy, "Rapid turnover of actin in dendritic spines and its regulation by activity," Nat. Neurosci., 5, No.3, 239-246 (2002).
69. O. Steward and E. M. Schuman, "Protein synthesis at synaptic sites on dendrites," Ann. Rev. Neurosci., 24, 299-325 (2001).
70. K. Svoboda, D. W. Tank, and W. Denk, "Direct measurement of coupling between dendritic spines neurons shafts," Science, 272, No.5262, 716-719 (1996).
71. E. Tanzi, "I fatti i le induzione nell'odierna istolgoia del sistema nervoso," Riv. Sper. Freniatri., 19, 419-472 (1893).
72. N. Toni, P. A. Buchs, I. Nikonenko, C. R. Bron, and D. Muller, "LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite," Nature, 402, No.6760, 421-425 (1999).
73. M. J. West, "Stereological methods for estimating the total number of neurons an synapses: Issues of precision and bias," Trends Neurosci., 22, No.2, 51-61 (1999).
74. C. S. Wolley and B. S. McEwen, "Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat," J. Neurosci., 12, No.7, 2549-2554 (1992).
75. M. Yankova, S. A. Hart, and C. S. Woolley, "Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: A serial electron-microscopic study," Proc. Natl. Acad. Sci. USA, 98, No.6, 3525-3530 (2001).
76. R. Yuste and T. Bonhoeffer, "Morphological changes in dendritic spins associated with long-term synaptic plasticity," Ann. Rev. Neurosci., 24, 1071-1089 (2001).
77. N. E. Ziv and S. J. Smith, "Evidence for a role of dendritic filopodia in synaptogenesis and spine formation," Neuron, 17, No.1, 91-1092 (1996).