Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro

Journal of Comparative Neurology

Volumn 465, Issue 1, 2003, Pages 90-103

  Fiala, John C ^a   Kirov, Sergei A ^b   Feinberg, Marcia D ^a   Petrak, Lara J ^a   George, Priya ^a   Goddard, C Alex ^a,c   Harris, Kristen M ^b,d  

^a Boston University   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Institute of Molecular Medicine and Genetics   (United States)

Author keywords

Coated vesicles; Dendrite; Dendritic spine; Depolymerization; Excitotoxicity; Glycogen; Interneuron; Ischemia; Metabolism; Microtubule; Synapse; Ultrastructure

Indexed keywords

GLYCOGEN;

ANIMAL CELL; ARTICLE; BRAIN PERFUSION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DEPOLYMERIZATION; GLIA; HIPPOCAMPUS; IN VITRO STUDY; INCUBATION TIME; ISCHEMIA; MALE; MICROTUBULE; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; SYNAPSE; TEMPERATURE DEPENDENCE; TISSUE FIXATION;

ANIMALS; CULTURE MEDIA; DENDRITES; DISSECTION; GLYCOGEN; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; INTERNEURONS; MALE; MICROSCOPY, ELECTRON; MICROTOMY; MICROTUBULES; NERVE DEGENERATION; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; OXYGEN; POSTMORTEM CHANGES; PRESYNAPTIC TERMINALS; RATS; RATS, LONG-EVANS; TISSUE FIXATION;

EID: 0043194092     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10825     Document Type: Article

References (66)

1. Aitken PG, Breese GR, Dudek FF, Edwards F, Espanol MT, Larkman PM, Lipton P, Newman GC, Nowak TS Jr, Panizzon KL, et al. 1995. Preparative methods for brain slices: a discussion. J Neurosci Methods 59:139-149.
2. Baas PW, Heidemann SR. 1986. Microtubule reassembly from nucleating fragments during the regrowth of amputated neurites. J Cell Biol 103:917-927.
3. Baas PW, Joshi HC. 1992. γ-Tubulin distribution in the neuron: implications for the origins of neuritic microtubules. J Cell Biol 119:171-178.
4. Banks P, Mayor D, Owen T. 1975. Effects of low temperatures on microtubules in the myelinated axons of post-ganglionic sympathetic nerves. Brain Res 83:277-292.
5. Barone FC, Feuerstein GZ, White RF. 1997. Brain cooling during transient focal ischemia provides complete neuroprotection. Neurosci Biobehav Rev 21:31-44.
6. Benveniste H, Drejer J, Schousboe A, Diemer NH. 1984. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374.
7. Benveniste H, Jorgensen MB, Diemer NH, Hansen AJ. 1988. Calcium accumulation by glutamate receptor activation is involved in hippocampal cell damage after ischemia. Acta Neurol Scand 78:529-536.
8. Benveniste H, Jorgensen MB, Sandberg M, Christensen T, Hagberg H, Diemer NH. 1989. Ischemic damage in hippocampal CA1 is dependent on glutamate release and intact innervation from CA3. J Cereb Blood Flow Metab 9:629-639.
9. Burgoyne RD, Gray EG, Sullivan K, Barron J. 1982. Depolymerization of dendritic microtubules following incubation of cortical slices. Neurosci Lett 31:81-85.
10. Cremona O, De Camilli P. 1997. Synaptic vesicle endocytosis. Curr Opin Neurobiol 7:323-330.
11. Croning MDR, Haddad GG. 1998. Comparison of brain slice chamber designs for investigations of oxygen deprivation in vitro. J Neurosci Methods 81:103-111.
12. Emery DG, Lucas JH. 1995. Ultrastructural damage and neuritic beading in cold-stressed spinal neurons with comparisons to NMDA and A23187 toxicity. Brain Res 692:161-173.
13. 2+ account for poor pyramidal cell structure in hippocampal slices. J Neurochem 55:473-483.
14. Feinberg MD, Szumowski KM, Harris KM. 2001. Microwave fixation of rat hippocampal slices. In: Giberson RT, Demaree RS, editors. Microwave techniques and protocols. Totowa, NJ: Humana Press. p 75-88.
15. Fiala JC, Harris KM. 1999. Dendrite structure. In: Stuart G, Spruston N, Häusser M, editors: Dendrites. Oxford, UK: Oxford University Press. p 1-34.
16. Fiala JC, Harris KM. 2001a. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J Microsc 202:468-472.
17. Fiala JC, Harris KM. 2001b. Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Informatics Assoc 8:1-16.
18. Folbergrova J, Li P-A, Uchino H, Smith M-L, Siesjo BK. 1997. Changes in the bioenergetic state of rat hippocampus during 2.5 minutes of ischemia, and prevention of cell damage by cyclosporin A in hyperglycemic subjects. Exp Brain Res 114:44-50.
19. Gulyás AI, Megías M, Emri Z, Freund TF. 1999. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of rat hippocampus. J Neurosci 19:10082-10097.
20. Hardham AR, Gunning BES. 1978. Structure of cortical microtubule arrays in plant cells. J Cell Biol 77:14-34.
21. Harris KM, Teyler TJ. 1984. Developmental onset of long-term potentiation in area CA1 of the rat hippocampus. J Physiol 346:27-48.
22. Heuser J. 1989. The role of coated vesicles in recycling of synaptic vesicle membrane. Cell Biol Int Rep 13:1063-1076.
23. Hillman DE. 1988. Parameters of dendritic shape and substructure: intrinsic and extrinsic determination? In: Lasek RL, Black MM, editors. Intrinsic determinants of neuronal form and function. New York: Alan R. Liss, Inc. p 83-113.
24. Jensen FE, Harris KM. 1989. Preservation of neuronal ultrastructure in hippocampal slices using rapid microwave-enhanced fixation. J Neurosci Methods 29:217-230.
25. Johnson OL, Ouimet CC. 2002. Protein synthesis is necessary for dendritic spine proliferation in vitro. Soc Neurosci Abst 153.5.
26. Jourdain P, Nikonenko I, Alberi S, Muller D. 2002. Remodeling of hippocampal synaptic networks by a brief anoxia-hypoglycemia. J Neurosci 22:3108-3116.
27. Kaech S, Parmar H, Roelandse M, Bornmann C, Matus A. 2001. Cytoskeletal microdifferentiation: a mechanism for organizing morphological plasticity in dendrites. Proc Natl Acad Sci USA 98:7086-7092.
28. Kiessling M, Stumm G, Xie Y, Herdegen T, Aguzzi A, Bravo R, Gass P. 1993. Differential transcription and translation of immediate early genes in the gerbil hippocampus after transient global ischemia. J Cereb Blood Flow Metab 13:914-924.
29. Kirov SA, Harris KM. 1999. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2:878-883.
30. Kirov SA, Sorra KE, Harris KM. 1999. Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876-2886.
31. Koizumi J. 1974. Glycogen in the central nervous system. Prog Histochem Cytochem 6:1-37.
32. Lipton P. 1988. Regulation of glycogen in the dentate gyrus of the in vitro guinea pig hippocampus: effect of combined deprivation of glucose and oxygen. J Neurosci Methods 28:147-154.
33. Lipton P, Aitken PG, Dudek FE, Eskessen K, Espanol MT, Ferchmin PA, Kelly JB, Kreisman NR, Landfield PW, Larkman PM, et al. 1995. Making the best of brain slices: comparing preparative methods. J Neurosci Methods 59:151-156.
34. Mandelkow EM, Mandelkow E, Milligan RA. 1991. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J Cell Biol 114:977-991.
35. McIlwain H, Tresize MA. 1956. The glucose, glycogen and aerobic glycolysis of isolated cerebral tissues. Biochem J 63:250-257.
36. McNiven MA, Porter KR. 1988. Organization of microtubules in centrosome-free cytoplasm. J Cell Biol 106:1593-1605.
37. Mies G, Kawai K, Saito N, Nagashima G, Nowak TS Jr, Ruetzler CA, Klatzo I. 1993. Cardiac arrest-induced complete cerebral ischaemia in the rat: dynamics of postischaemic in vivo calcium uptake and protein synthesis. Neurol Res 15:253-263.
38. Morin F, Crevier C, Bouvier G, Lacaille J-C, Beaulieu C. 1997. A fixation procedure for ultrastructural investigation of synaptic connections in resected human cortex. Brain Res Bull 44:205-210.
39. Newman GC, Qi H, Hospod FE, Grundmann K. 1992. Preservation of hippocampal brain slices with in vivo or in vitro hypothermia. Brain Res 575:159-163.
40. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system, 3rd ed, New York: Oxford University Press.
41. Piccini A, Malinow R. 2001. Transient oxygen-glucose deprivation induces rapid morphological changes in rat hippocampal dendrites. Neuropharmacology 41:724-729.
42. Sasaki S, Steven JK, Bodick N. 1983. Serial reconstruction of microtubular arrays within dendrites of the cat retinal ganglion cell: the cytoskeleton of a vertebrate dendrite. Brain Res 259:193-206.
43. Schulze E, Kirschner M. 1988. New features of microtubule behaviour observed in vivo. Nature 334:356-359.
44. Schurr A, Reid KH, Tseng MT, Edmonds HL Jr. 1984. The stability of the hippocampal slice preparation: an electrophysiological and ultrastructural analysis. Brain Res 297:357-362.
45. Schurr A, Teyler TJ, Tseng MT. 1987. Brain slices: fundamentals, applications and implications. Basel: Karger.
46. Schurr A, Payne RS, Miller JJ, Rigor BM. 1997. Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res 774:221-224.
47. Schurr A, Miller JJ, Payne RS, Rigor BM. 1999. An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons. J Neurosci 19:34-39.
48. + and water during the first two hours of in vitro incubation of hippocampal slices. Neuroscience 79:1013-1022.
49. Spacek J. 1985. Three-dimensional analysis of dendritic spines. II. Spine apparatus and other cytoplasmic components. Anat Embryol 171:235-243.
50. Staff NP, Jung HY, Thiagarajan T, Yao M, Spruston N. 2000. Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. J Neurophysiol 84:2398-2408.
51. Stevens JK, Trogadis J, Jacobs JR. 1988. Development and control of axial neurite form: a serial electron microscopic analysis. In: Lasek RL, Black MM, editors. Intrinsic determinants of neuronal form and function. New York: Alan R. Liss, Inc. p 115-145.
52. Taubenfeld SM, Stevens KA, Pollonini G, Ruggiero J, Alberini CM. 2002. Profound molecular changes following hippocampal slice preparation: loss of AMPA receptor subunits and uncoupled mRNA/protein expression. J Neurochem 81:1348-1360.
53. Tian G-F, Baker AJ. 2000. Glycolysis prevents anoxia-induced synaptic transmission damage in rat hippocampal slices. J Neurophysiol 83:1830-1839.
54. Troutt LL, Wang E, Pagh-Roehl K, Burnside B. 1990. Microtubule nucleation and organization in teleost photoreceptors: microtubule recovery after elimination by cold. J Neurocytol 19:213-223.
55. Van Rossum D, Hanisch U-K. 1999. Cytoskeletal dynamics in dendritic spines: direct modulation by glutamate receptors? TINS 22:290-295.
56. Wang J, Yu W, Baas PW, Black MM. 1996. Microtubule assembly in growing dendrites. J Neurosci 16:6065-6078.
57. Weisenberg RC, Deery WJ. 1981. The mechanisms of calcium-induced microtubule disassembly. Biochem Biophys Res Commun 102:924-931.
58. Wenzel J, Otani S, Desmond NL, Levy WB. 1994. Rapid development of somatic spines in stratum granulosum of the adult hippocampus in vitro. Brain Res 656:127-134.
59. Westrum LE, Jones DH, Gray EG, Barron J. 1980. Microtubules, dendritic spines and spine apparatuses. Cell Tissue Res 208:171-181.
60. Whittingham TS, Lust WD, Christakis DA, Passonneau JV. 1984. Metabolic stability of hippocampal slice preparations during prolonged incubation. J Neurochem 43:689-696.
61. Xu ZC, Pulsinelli WA. 1994. Responses of CA1 pyramidal neurons in rat hippocampus to transient forebrain ischemia: an in vivo intracellular recording study. Neurosci Lett 171:187-191.
62. Yamamoto K, Morimoto K, Yanagahara T. 1986. Cerebral ischemia in the gerbil: transmission electron microscopic and immunoelectron microscopic investigation. Brain Res 384:1-10.
63. Yamane K, Yokono K, Okada Y. 2000. Anaerobic glycolysis is crucial for the maintenance of neural activity in guinea pig hippocampal slices. J Neurosci Methods 103:163-171.
64. Yu W, Cook C, Sauter C, Kuriyama R, Kaplan PL, Baas PW. 2000. Depletion of a microtubule-associated motor protein induces the loss of dendritic identity. J Neurosci 20:5782-5791.
65. 2+ release from mitochondria. J Neurosci 19:3307-3315.
66. Zhou Q, Abe H, Nowak TS Jr. 1995. Immunocytochemical and in situ hybridization approaches to the optimization of brain slice preparations. J Neurosci Methods 59:85-92.