The effect of aging-associated impaired mitochondrial status on kainate-evoked hippocampal gamma oscillations

Neurobiology of Aging

Volumn 33, Issue 11, 2012, Pages 2692-2703

  Lu, Cheng B ^a   Vreugdenhil, Martin ^a   Toescu, Emil C ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Calcium signal; Gamma oscillations; Kainate; Mitochondrial depolarization; Mitochondrial protonophore

Indexed keywords

CALCIUM; KAINIC ACID; RHODAMINE 123;

AGING; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CALCIUM SIGNALING; COGNITION; DEPOLARIZATION; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NERVE CELL NETWORK; NEUROIMAGING; NEUROMODULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; TASK PERFORMANCE;

AGING; ANIMALS; CALCIUM; ELECTROPHYSIOLOGICAL PHENOMENA; HIPPOCAMPUS; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NEURONS;

EID: 84865602861     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.01.001     Document Type: Article

References (75)

1. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
2. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., Kandel E.R. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5280-5285.
3. Barth A.M.I., Mody I. Changes in hippocampal neuronal activity during and after unilateral selective hippocampal ischemia in vivo. J Neurosi 2011, 31:851-860.
4. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci 2007, 8:45-56.
5. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol 2005, 58:495-505.
6. Bindokas V., Lee C., Colmers W., Miller R. Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci 1999, 18:4570-4587.
7. Boumezbeur F., Mason G.F., de Graaf R.A., Behar K.L., Cline G.W., Shulman G.I., Rothman D.L., Petersen K.F. Altered brain mitochondrial metabolism in healthy aging as assessed by in vivo magnetic resonance spectroscopy. J. Cereb. Blood Flow Metab 2010, 30:211-221.
8. Boveris A., Navarro A. Brain mitochondrial dysfunction in aging. IUBMB Life 2008, 60:308-314.
9. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci 1995, 15:47-60.
10. Brustovetsky N., Dubinsky J.M. Dual responses of CNS mitochondria to elevated calcium. J. Neurosci 2000, 20:103-113.
11. Buzsáki G., Buhl D.L., Harris K.D., Csicsvari J., Czéh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 2003, 116:201-211.
12. Caeser M., Aertsen A. Morphological organization of rat hippocampal slice cultures. J. Comp. Neurol 1991, 307:87-106.
13. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
14. De Stefani D., Raffaello A., Teardo E., Szabò I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
15. Dickinson R., Awaiz S., Whittington M.A., Lieb W.R., Franks N.P. The effects of general anaesthetics on carbachol-evoked gamma oscillations in the rat hippocampus in vitro. Neuropharmacology 2003, 44:864-872.
16. Driver J.E., Racca C., Cunningham M.O., Towers S.K., Davies C.H., Whittington M.A., LeBeau F.E. Impairment of hippocampal gamma-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur. J. Neurosci 2007, 26:1280-1288.
17. Duchen M.R. Ca(2+)-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J 1992, 283:41-50.
18. Egebjerg J., Heinemann S.F. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:755-759.
19. Erickson C.A., Barnes C.A. The neurobiology of memory changes in normal aging. Exp. Gerontol 2003, 38:61-69.
20. Fisahn A. Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool. J. Physiol 2005, 562:65-72.
21. Fisahn A., Contractor A., Traub R.D., Buhl E.H., Heinemann S.F., McBain C.J. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J. Neurosci 2004, 24:9658-9668.
22. Fisahn A., Pike F.G., Buhl E.H., Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 1998, 394:186-189.
23. Fries P., Nikolić D., Singer W. The gamma cycle. Trends Neurosci 2007, 30:309-316.
24. 2+ transients. Biochim. Biophys. Acta 1998, 1366:5-15.
25. Hagen T.M., Yowe D.L., Bartholomew J.C., Wehr C.M., Do K.L., Park J.Y., Ames B.N. Mitochondrial decay in hepatocytes from old rats: Membrane potential declines, heterogeneity and oxidants increase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:3064-3069.
26. Hájos N., Ellender T.J., Zemankovics R., Mann E.O., Exley R., Cragg S.J., Freund T.F., Paulsen O. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur. J. Neurosci 2009, 29:319-327.
27. Hájos N., Pálhalmi J., Mann E.O., Németh B., Paulsen O., Freund T.F. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J. Neurosci 2004, 24:9127-9137.
28. Hedden T., Gabrieli J.D. Insights into the ageing mind: a view from cognitive neuroscience. Nat. Rev. Neurosci 2004, 5:87-96.
29. Hoyt K.R., Stout A.K., Cardman J.M., Reynolds I.J. The role of intracellular Na+ and mitochondria in buffering of kainate-induced intracellular free Ca2+ changes in rat forebrain neurones. J. Physiol 1998, 509:103-116.
30. 2 and concomitant changes in mitochondrial redox state. J. Neurosci 2008, 28:1153-1162.
31. Kann O., Huchzermeyer C., Kovács R., Wirtz S., Schuelke M. Gamma oscillations in the hippocampus require high complex I gene expression and strong functional performance of mitochondria. Brain 2011, 134:345-358.
32. Kann O., Kovács R. Mitochondria and neuronal activity. Am. J. Physiol. Cell Physiol 2007, 292:C641-C657.
33. Kirichok Y., Krapivinsky G., Clapham D.E. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 2004, 427:360-364.
34. Kovács R., Kardos J., Heinemann U., Kann O. Mitochondrial calcium ion and membrane potential transients follow the pattern of epileptiform discharges in hippocampal slice cultures. J. Neurosci 2005, 25:4260-4269.
35. Kunz W.S., Goussakov I.V., Beck H., Elger C.E. Altered mitochondrial oxidative phosphorylation in hippocampal slices of kainate-treated rats. Brain Res 1999, 826:236-242.
36. LaFrance R., Brustovetsky N., Sherburne C., Delong D., Dubinsky J.M. Age-related changes in regional brain mitochondria from Fischer 344 rats. Aging Cell 2005, 4:139-145.
37. Lerma J. Kainate receptor physiology. Curr. Opin. Pharmacol 2006, 6:89-97.
38. Lisman J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 1999, 22:233-242.
39. Lu C.B., Hamilton J.B., Powell A.D., Toescu E.C., Vreugdenhil M. Effect of ageing on CA3 interneuron sAHP and gamma oscillations is activity-dependent. Neurobiol Aging 2011, 32:956-965.
40. Lu C.B., Jefferys J.G., Toescu E.C., Vreugdenhil M. In vitro hippocampal gamma oscillation power as an index of in vivo CA3 gamma oscillation strength and spatial reference memory. Neurobiol. Learn. Mem 2011, 95:221-230.
41. Ma J., Leung L.S. Relation between hippocampal gamma waves and behavioral disturbances induced by phencyclidine and methamphetamine. Behav. Brain Res 2000, 111:1-11.
42. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J. Exp. Biol 2006, 209:2304-2311.
43. Mathew S.S., Hablitz J.J. Calcium release via activation of presynaptic IP3 receptors contributes to kainate-induced IPSC facilitation in rat neocortex. Neuropharmacology 2008, 55:106-116.
44. Mattson M.P., Gleichmann M., Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766.
45. McEchron M.D., Weible A.P., Disterhoft J.F. Aging and Learning-Specific Changes in Single-Neuron Activity in CA1 Hippocampus During Rabbit Trace Eyeblink Conditioning. J. Neurophysiol 2001, 86:1839-1857.
46. Moreau B., Nelson C., Parekh A.B. Biphasic regulation of mitochondrial Ca2+ uptake by cytosolic Ca2+ concentration. Curr. Biol 2006, 16:1672-1677.
47. Navarro A., Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol 2007, 292:C670-C686.
48. Navarro A., López-Cepero J.M., Bández M.J., Sánchez-Pino M.J., Gómez C., Cadenas E., Boveris A. Hippocampal mitochondrial dysfunction in rat aging. Am. J. Physiol. Regul. Integr. Comp. Physiol 2008, 294:R501-R509.
49. 2+]i and membrane currents during impaired mitochondrial metabolism in dissociated rat hippocampal neurons. J. Physiol 1998, 507:131-145.
50. Parihar M.S., Brewer G.J. Simultaneous age-related depolarization of mitochondrial membrane potential and increased mitochondrial reactive oxygen species production correlate with age-related glutamate excitotoxicity in rat hippocampal neurons. J. Neurosci. Res 2007, 85:1018-1032.
51. Peng T.I., Greenamyre J.T. Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol. Pharmacol 1998, 53:974-980.
52. Peterlin Z.A., Kozloski J., Mao B.Q., Tsiola A., Yuste R. Optical probing of neuronal circuits with calcium indicators. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:3619-3624.
53. Rasmussen T., Schliemann T., Sørensen J.C., Zimmer J., West M.J. Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol. Aging 1996, 17:143-147.
54. Rego A.C., Ward M.W., Nicholls D.G. Mitochondria control AMPA/Kainate receptor-induced cytoplasmic calcium deregulation in rat cerebellar granule cells. J. Neurosci 2001, 21:1893-1901.
55. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol 2003, 69:143-179.
56. Ruiz A., Sachidhanandam S., Utvik J.K., Coussen F., Mulle C. Distinct subunits in heteromeric kainate receptors mediate ionotropic and metabotropic function at hippocampal mossy fiber synapses. J. Neurosci 2005, 25:11710-11718.
57. Sakatani S., Seto-Ohshima A., Shinohara Y., Yamamoto Y., Yamamoto H., Itohara S., Hirase H. Neural-activity-dependent release of S100B from astrocytes enhances kainate-induced gamma oscillations in vivo. J. Neurosci 2008, 28:10928-10936.
58. Shuttleworth C.W., Brennan A.M., Connor J.A. NAD(P)H fluorescence imaging of postsynaptic neuronal activation in murine hippocampal slices. J. Neurosci 2003, 23:3196-3208.
59. Thibault O., Gant J.C., Landfield P.W. Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell 2007, 6:307-317.
60. Thibault O., Hadley R., Landfield P.W. Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J. Neurosci 2001, 21:9744-9756.
61. Toescu E.C. Mitochondria and Ca(2+) signaling. J. Cell. Mol. Med 2000, 4:164-175.
62. Toescu E.C. Normal brain ageing: Models and Mechanisms. Philos. Trans. R. Soc. Lond 2005, 360:2347-2354.
63. Toescu E.C., Verkhratsky A. Assessment of mitochondrial polarization status in living cells based on analysis of the spatial heterogeneity of rhodamine 123 fluorescence staining. Pflugers Arch 2000, 440:941-947.
64. Toescu E.C., Verkhratsky A. The importance of being subtle: small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell 2007, 6:267-273.
65. Toescu E.C., Verkhratsky A., Landfield P.W. Ca2+ regulation and gene expression in normal brain aging. Trends Neurosci 2004, 27:614-620.
66. Toescu E.C., Vreugdenhil M. Calcium and normal brain ageing. Cell Calcium 2010, 47:158-164.
67. Turner J.G., Hughes L.F., Caspary D.M. Affects of aging on receptive fields in rat primary auditory cortex layer V neurons. J. Neurophysiol 2005, 94:2738-2747.
68. Uchida S., Nakayama H., Maehara T., Hirai N., Arakaki H., Nakamura M., Nakabayashi T., Shimizu H. Suppression of gamma activity in the human medial temporal lobe by sevoflurane anesthesia. Neuroreport 2000, 11:39-42.
69. Vergun O., Keelan J., Khodorov B.I., Duchen M.R. Glutamate-induced mitochondrial depolarisation and perturbation of calcium homeostasis in cultured rat hippocampal neurones. J. Physiol 1999, 519:451-466.
70. Vreugdenhil M., Toescu E.C. Age-dependent reduction of gamma oscillations in the mouse hippocampus in vitro. Neuroscience 2005, 132:1151-1157.
71. Ward M.W., Rego A.C., Frenguelli B.G., Nicholls D.G. Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci 2000, 20:7208-7219.
72. 2+]i signalling in rat cerebellar granule neurones aged in vitro. Neurobiol. Aging 2004, 25:349-359.
73. Xiong J., Verkhratsky A., Toescu E.C. Changes in mitochondrial status associated with altered Ca2+ homeostasis in aged cerebellar granule neurons in brain slices. J. Neurosci 2002, 22:10761-10771.
74. Yang Y., Liang Z., Li G., Wang Y., Zhou Y. Aging affects response variability of V1 and MT neurons in rhesus monkeys. Brain Res 2009, 1274:21-27.
75. Young K.W., Bampton E.T., Pinòn L., Bano D., Nicotera P. Mitochondrial Ca2+ signalling in hippocampal neurons. Cell Calcium 2008, 43:296-306.